Chromosomal rearrangements as speciation mechanisms - CRC Thesis

“Chromosomal rearrangements as speciation mechanisms” – Cino Robin Castelli
Universita’ degli Studi Milano Bicocca – Master’s Degree Thesis in Molecular Biology
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REVISION 8.1
Chromosomal rearrangements as speciation mechanisms
Master’s Degree Thesis in Molecular Biology
Universita’ degli Studi Milano Bicocca
Author:
Cino Robin Castelli
Matricola.: 032266
Thesis advisor: Prof. Maurizio Casiraghi
Thesis Co-Advisor: Prof. Sergio Ottolenghi
Thesis dissertation date: October 9th
, 2015
Degree in: Biological Sciences N. O.
Last Update: September 23rd
, 2015
Copyright ©
Cino Robin Castelli 2015

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INDEX
1.1. ABSTRACT 7
1.2. INTRODUCTION 10
1.2.1. Concept of Species 10
1.2.1.1. Linnaean and early Darwinian definitions of species 10
1.2.1.2. Biological Species Concept (BSC) I – (Dobzhansky 1937, 1970, Mayr 1942, 1963) 10
1.2.1.3. Biological Species Concept (BSC) II – (Mayr 1982) 11
1.2.1.4. The recognition species concept – (Paterson 1978, 1985) 12
1.2.1.5. The cohesion species concept – (Templeton 1989) 13
1.2.1.6. The Evolutionary species concept by Simpson – (Simpson 1961) 14
1.2.1.7. The Evolutionary species concept by Wiley– (Wiley 1978) 15
1.2.1.8. The Ecological species concept – (Van Halen 1976) 16
1.2.1.9. The Phylogenetic species concept – (Cracraft 1983) 17
1.2.1.10. Species concept as used in this publication 18
1.2.2. Historical views on chromosomal speciation 19
1.2.3. Frequency of chromosomal rearrangements 20
1.2.3.1. Types of negatively heterotic chromosomal rearrangements 23
1.2.3.2. Fertility effects of balanced chromosomal translocations on carriers 24
1.2.4. Chromosomal differences between closely related species in nature and among domesticated animals 29
1.2.4.1. Examples of hybrid sterility and reduced viability in hybrids 31
1.3. Methods for predicting fixation of chromosomal translocations 33
1.3.1. The role of population size 34
1.3.1.1. The role of small, locally isolated populations 36
1.3.1.2. The role of the founder effect 36
1.3.1.3. Effects of mating with members of the wild type species 38
1.3.2. The reinforcement hypothesis 38
1.3.2.1. The theoretical foundation of a species reinforcement gene 39
1.3.2.2. Reinforcement model via refusal to mate with WT individuals alone 39
1.3.2.3. Reinforcement model via refusal to mate with WT individuals and hybrids 40
1.3.2.4. Reinforcement via sexual mate selection genes or SMRS complexes 40
2. MATERIALS, METHODS AND RESULTS 41
2.1. HARDY-WEINBERG EXPANSION FOR TWO GENES, RANDOM MATING, NO SELECTION: 41
2.2. HARDY WEINBERG EXPANSION FOR TWO GENES, SEXUAL SELECTIVE MATING, R gene rejects mating
exclusively with WW genotype: 50
2.3. HARDY WEINBERG EXPANSION FOR TWO GENES, SEXUAL SELECTIVE MATING, R gene rejects mating both with
WW genotype and WN genotype: 63
2.4. Computer Simulation results, Simple translocation without immigration from WW individuals: 70
2.5. Computer Simulation results, Simple translocation with immigration from WW individuals, variable influx of
migration (simulations with NN population collapse were repeated 10 times for statistical significance): 77
2.6. Computer Simulation results, Simple translocation with immigration from WW individuals, no influx of
migration, occurrence of R gene at variable starting frequencies: 99
migration, occurrence of R gene at variable starting frequencies, different numbers of generations, R GENE ONLY
REFUSES WT MATINGS: 109

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migration, occurrence of R gene at variable starting frequencies, different numbers of generations, R GENE REJECTS WW
AND WN GENOTYPES: 126
2.9. MATLAB CODE: 134
2.10. Translocated modified HW Equilibrium with influx of WT migrants: 134
2.11. Translocated modified HW Equilibrium with influx of WT migrants and R gene refusing to mate with WW
individuals (gene is dominant, does not refuse mating with WN individuals): 139
2.12. Translocated modified HW Equilibrium with influx of WT migrants and R gene refusing to mate with WW and
WN individuals (gene is dominant): 146
3. DISCUSSION 154
3.1. Results of computer simulations 154
3.1.1. The instability of translocations as polymorphisms 158
3.1.1.1. Fixed translocations between populations must represent speciation events 158
3.1.1.2. Factors affecting fixation versus extinction 159
3.1.1.3. Resistance to introgression once fixation is achieved 162
3.1.2. The reinforcement hypothesis, pure WT refusal 162
3.1.2.1. Instauration of a new equilibrium that provides optimal fitness 163
3.1.2.2. Number of generations required to instauration of equilibrium 163
3.1.2.3. Resistance to introgression from WT individuals 164
3.1.3. The reinforcement hypothesis, pure WT and hybrid refusal 164
3.1.3.1. Instauration of a new equilibrium that provides optimal fitness 164
3.1.3.2. Number of generations required to instauration of equilibrium 165
3.1.3.3. Resistance to introgression from WT individuals 165
3.2. Theoretical Implications of Chromosomal speciation model 165
3.2.1. The instability of balanced translocations as polymorphisms 165
3.2.2. Micromutation vs. Macromutation 165
3.2.3. Neomutation, drift and selection 166
3.2.4. Meiotic drive 166
3.2.5. Evolutionary advantage of sexual reproduction 167
3.2.6. Adaptive value of speciation 167
3.2.7. Gene flow acting against reinforcement 167
3.2.8. Extinction versus speciation 168
3.2.9. Probability of chromosomal speciation 168
4. CITATIONS 169

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REVISIONS
REVISION DATE
(dd-mm-yyyy)
COMMENTS
1.0 09-07-2015 First draft of structure.
1.1 16-07-2015 Updated title, added notes.
3.0 19-08-2015 Inserted correct equations for reinforcement case.
4.0 24-08-2015 Corrected equation mating factors.
5.1 15-09-2015
Moved equations to methodology, expanded
abstract.
5.2 16-09-2015
Finished species concept section, elaborated
chromosome rearrangement section.
5.3 17-09-2015
Finished chromosome rearrangement section.
Finished Chromosomal differences section.
Expanded effect of hybridization section.
5.4 18-09-2015 Finished introduction chapter.
6.1 19-09-2015
Reviewed and corrected theoretical modeling section
for Reinforcement scenario.
6.2 20-09-2015
Included final models and code for WN and WT
refusal reinforcement models.
6.3 21-09-2015 Expanded discussion section.
6.4 22-09-2013 Finished discussion section.
7.0 22-09-2013 First version for proof-reading.
8.0 22-09-2013 Final revision.
8.1 23-09-2013 Corrected minor typographical errors.

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Table 1 – Reference Publications
Ref
Number
Publication
1
Darwin, C. – On the origin of species or the preservation of favoured
races in the struggle for life – John Murray, Albemarle Street. Down,
Bromley, Kent,1859.
2 R.A. Fisher – The Genetical Theory of Natural Selection – Oxford at the
Clarendon Press – 1930 – ISBN 978-1-31402-967-3.
3 A. Fontdevila - Evolutionary Biology of Transient Unstable Populations -
Springer 1990 - ISBN-0-38-750837-6.
4 D.L. Hartl & A.G. Clark – Principles of Population Genetics, fourth edition
– Sinauer Associates 2007 – ISBN 978-0-87893-308-2.
5 D.J. Howard & S.H. Berlocher (Editors) - Endless Forms, Species and
Speciation -Oxford University Press 1998 - ISBN 0-19-510901-5.
6 M. King - Species Evolution: The Role of Chromosome Change -
Cambridge University Press 1995 - ISBN 0-521-48454-5.
7 J.S. Levinton - Genetics, Palaeontology and Macroevolution, Second
Edition - Cambridge University Press 2001 - ISBN 0-521-00550-7.
8 J. Maynard Smith - Evolution and the Theory of Games - Cambridge
University Press 1982 - ISBN 0-521-28884-3.
9 J. Maynard Smith - Evolutionary Genetics, Second Edition - Oxford
University Press 1998 - ISBN 0-19-850231-1.
10 J. Maynard Smith & E. Szathmary - The Major Transitions in Evolution -
Oxford University Press 1995 - ISBN 0-19-850294-X.
11 E. Mayr - The Growth of Biological Thought, Diversity Evolution and
Inheritance - Harvard University Press 1982 - ISBN 0-674-36446-5.
12 R.E. Michod - Darwinian Dynamics, Evolutionary Transitions in Fitness
and Individuality - Princeton Paperbacks 2000 - ISBN 0-691-05011-2.
13 O.J. Miller & E. Therman - Human Chromosomes, fourth edition - Springer
2001 - ISBN 0-387-95046-X.

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14 M. Mitchell - An Introduction to Genetic Algorithms - MIT Press 1996 -
ISBN 0-262-63185-7.
15 M. Nitecki (Editor) – Evolutionary Progress – The University of Chicago
Press, Chicago and London 1988 - ISBN 0-226-58692-8.
16 M.Ridley (Editor) - Evolution - Oxford University Press 1997 - ISBN 0-19-
289287-8.
17 Q.D. Wheeler & R. Meier (Editors) - Species Concept and Phylogenetic
Theory, a Debate - Columbia University Press 2000 - ISBN 0-231-10143-0.
18 M. J. D. White - Animal Cytology and Evolution - Cambridge University
Press 1945 - ISBN 0-521-07071-6.
19 R.A. Wilson (Editor) - Species, New Interdisciplinary Essays - MIT Press
1999 - ISBN 0-262-23201-4.
20
S. Wright – Evolution and the Genetics of populations. Volume 4,
Variability within and among Natural Populations – The University of
Chicago Press, Chicago and London 1978 - ISBN 0-226-91041-5.

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1.1. ABSTRACT
Since the beginning of early evolutionary studies, in fact since Darwin himself in his most famous work,
“On the Origin of Species”, biologists have been trying to answer the question of how species arise and
how they can achieve the necessary reproductive barriers that are required to allow mutation and
selection to operate and differentiate a neo-species from the mother species.
It is an accepted tenet of evolutionary biology that species evolve into new species which are direct
descendants of the original species. The closer the relationship between species is, the higher the
percentage of genetic homology is. Closely related species often show extremely high levels of genetic
homology (at times as high as what is measured between local populations within the same species)
while differing by balanced chromosomal rearrangements.
The theory of chromosomal speciation has been often proposed as a mechanism for new species
emergence and the subject of this thesis is a novel approach to analysis and theoretical modeling of
how it operates, and how certain categories of mutations can reinforce its effects.
Translocation and chromosomal rearrangements occur in all eukaryotes with measurable and relatively
fixed probabilities. Chromosomal rearrangements are one-time single events that occur in one specific
individual during gametogenesis and are a common type of mutation. They can affect the Darwinian
fitness of the affected individual in a significant manner if the individual is mating with non-rearranged
individuals as follows.
In the case of translocated individuals, gametes show reduced fertility when crossed with non-
rearranged individuals. This decrease in fertility is quantified as ½ for crosses between rearranged
heterozygotes and Wild Type or rearranged homozygotes, and is due to unbalanced gametes resulting
from incorrect segregation during meiosis. The decrease in fertility for crosses between rearranged
heterozygotes is even higher (the resulting fertility of these crosses is 5/16, making the reduction in
fertility 11/16) due to the possible combinations between gametes and the resulting imbalances.
Within large interbreeding populations, due to the validity of the Hardy-Weinberg law, chromosomal
rearrangements are lost from the gene pool in one or very few generations due to their negatively
heterotic effect on the fitness of individuals carrying these mutations (negatively heterotic meaning it
negatively affects the fitness of the heterozygote). Hardy-Weinberg equilibria are also the reason that,
in large populations, evolution of new characteristics is very slow (becoming increasingly slower in
proportion to the size of the population, reaching theoretical zero evolutionary speed for an infinitely
large freely interbreeding population).
Amongst all the possible chromosomal rearrangements, some are negatively heterotic while others are
neutral or potentially positively heterotic (in a limited number of cases). This thesis focuses exclusively
on the negatively heterotic rearrangements, since they are the only ones that can play a leading role in
speciation, and will not go into details on the other rearrangements that are expected to be present in
populations as polymorphisms that play no significant role in speciation.
If we examine locally isolated populations, characterized by inbreeding and, potentially, founder effects,
we observe how, through stochastic processes, fixation of negatively heterotic chromosomal
rearrangements can occur. It is important to note how, in order for local fixation to occur, the size of the
population must be very small (fixation relies on genetic drift and stochastic factors that become
extremely improbable when the number of interbreeding members of the population increases). If a
chromosomal rearrangement becomes fixed in a small population, this population will be characterized

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by having very similar genotypes which will be to some extent different from the average allelic
frequencies within the founder population. This difference will be proportional to the variance in the
original population.
Amongst the negatively heterotic chromosomal rearrangements (nominally Tandem Fusions,
Robertsonian Fusions, Reciprocal Translocations, X-autosome translocations, and, potentially, multiple
inversions) we shall focus on Reciprocal Translocations, for which a theoretical model will be
presented.
Once a negatively heterotic chromosomal rearrangement has become fixed in a local population, if the
new population has limited and sporadic interbreeding with the founder population, the members that
breed with the founding population members will have a lower fitness than those who do not do so (this
has been called the “reinforcement hypothesis”). As a result of this hypothesis, it has been proposed
that, over a limited number of generations, strong mating barriers will evolve.
A strong candidate for the reinforcement mechanism is represented by genes that control visible
factors that differentiate the new population from the old, such as secondary sexual characters, which
will be favorably selected if they distinguish the new population from the founding population and
increase reproductive isolation. It is therefore proposed that the new population will rapidly evolve
different secondary sexual characteristics as a result of this.
By modification of the Hardy Weinberg equilibrium we can model the effects of hybridization and influx
of Wild Type individuals into the new population. A modified version of the Hardy-Weinberg equilibrium
is presented in this thesis which includes both the effect of the translocation and the effects of the
translocation coupled with the emergence of reinforcement genes. Computer models based on these
matings have been developed for this thesis and will be presented.
The results of the simulations show how the founding population and the new population will either
merge (in which case the new population will be absorbed into the founding population and the
rearrangement will disappear within very few generations) or drift apart and become completely
separate, non-interbreeding (or minimally interbreeding) populations.
The model also shows how, when a population fixes a chromosomal translocation, it becomes very
resistant to re-invasion by the WT karyotype, and shows the capability of resisting repeat influx of up to
4.0% of the entire population per generation by WT individuals without extinction.
Higher percentages, however, rapidly result in the extinction of the NS karyotype (3/10 cases in up to
4.5% random influx per generation resulted in extinction before 10.000 generations and 10/10 when the
random influx is raised to up to 5%).
Once reinforcement genes appear, the model shows how they rapidly become established, albeit not
fixated, in the population, and generate a much stronger barrier to introgression by WT individuals.
The results of these simulations show how, once a rearranged population for a negatively heterotic
chromosomal rearrangement has separated itself from the original population, such as described
above, it only has two possible pathways available. The first is the pathway towards becoming a new
species while the second is the one leading to extinction of the rearrangement and reabsorption into
the original population.
Given that translocations either disappear or give rise to new species, each translocation event that
can be determined to exist between two related species must represent a single speciation event.
As a side note, this mechanism points to how the evolutionary significance of Sexual reproduction lies
in the fact that sexual populations are capable of speciation, while asexual ones are not. Sexual

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reproduction thus allows for adaptation through speciation and radiation. In a nutshell, speciation exists
because of sexual reproduction and vice versa.
Since sexually reproducing species can radiate by chromosomal speciation into different species, the
existence of sexual reproduction provides a clear evolutionary advantage that offsets the associated
costs.
New species can adapt and respond quicker to evolutionary pressure due to the lower numbers that
allow quicker fixation of beneficial mutations compared to large populations. They are, however, more
prone to the risk of extinction (i.e. it’s an “all or nothing” game, where most newly formed chromosomal
species will become rapidly extinct). Paradoxically, large interbreeding populations, which would be
considered an evolutionary success, pay for this success by losing the capability to speciate.
In large interbreeding populations, evolution only happens in response to large disruptions (epidemics,
pandemics, food shortages leading to mass mortality, etc…) or over extremely long timeframes and
numbers of generations.
The proposed model can be further reinforced if the translocations occur in dominant males in small
populations causing a higher chance of leading to speciation.
The path to speciation begins with the appearance of a F1 generation of NS/WT hybrids followed,
through inbreeding, by the appearance of homozygous NS/NS individuals in the F2 generation.
Stochastic factors play a large role in this stage, with the general characteristic of the probability of
speciation being very low in absolute terms.
The study of statistics however teaches us that, in evolutionary terms, very low probability events
happen all the time.
Speciation events thus are an overall rare event which happens with variable frequencies based on the
characteristics of the species of origin (habitat, mobility, reproductive mechanisms, etc…). Each of
these characteristics can have major effect on the number of species that evolve within closely related
taxa (thus providing an explanation for taxa where speciation appears to be a very common thing and
taxa which appear unchanged and composed of a very limited number of species for millions or tens of
millions of years).

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1.2. INTRODUCTION
1.2.1. Concept of Species
Multiple species concepts have been proposed since before Darwin (1859) first published the “Origin of
Species” and the true meaning of the term species is one of the most hotly debated issues within
biology.
Mirroring the various positions that are present in the scientific community on this subject, it is
acceptable to state that “the unit of evolution is the terminal taxon, the isolated interbreeding population
which is an objective reality. All living beings belong to a terminal taxon, but whether or not a given
species is a terminal taxon is unpredictable, being dependent on future discovery”, as Lovtrup (1979,p.
388) postulated.
We shall rapidly review the most relevant proposed species definitions, using the excellent trace laid
out by Max King in “Species Evolution - The role of chromosome change” (King 1993), and will then
proceed to explain the choice of the one that is utilized in the course of this publication.
1.2.1.1. Linnaean and early Darwinian definitions of species
The earliest modern concepts of species would not survive any degree of scrutiny today. If we
examine the taxonomical method used by Linnaeus (1751), who described species based on
morphological similarities, and we then fast forward in time to Agassiz (1857) who added a
philosophical/religious aspect to the categorization of nature (Agassiz defined a species as
“thoughts of the creator which are real”) we see how the very nature of what constitutes a
species was nebulous since the beginning of modern biological thought. Darwin’s own view of
the concept of species, and its origin, is very primordial and would gain very little acceptance in
the modern scientific community. Darwin specifically didn’t address the actual problem of the
origin of species as such in his seminal work, concentrating instead on the concept of evolution
seen as the differential survival of the fittest within the loosely defined concept of species (and
thus giving origin to modern evolutionary thought). Darwin considered species as open systems
with fluid borders that could only subjectively be delimited (King, 1993).
The concept of “morphospecies” was the de facto standard for over two centuries, between the
publication of Linnaeus’ “Systema Naturae” in 1735 and the emergence of the biological species
concept in the late 1950’s.
It is surprising how a true, biologically based debate on the definition of species didn’t occur until
the second half of the twentieth century when a generation of biologists started applying the
ever-growing knowledge of genetics, molecular biology and cytogenetics to the age-old problem
of species. This generation of biologists was led by Ernst Mayr and Theodosius Dobzhansky and
formed the basis for the current modern species concepts.
1.2.1.2. Biological Species Concept (BSC) I – (Dobzhansky 1937, 1970, Mayr 1942, 1963)
The first challenge to the established morphological concept of species was brought forth by
Dobzhansky in 1937 when he pointed out that the process responsible for species formation was
the development of reproductive isolating mechanisms, thus linking the possibility of
interbreeding and producing fertile offspring to the concept of species, independently of the
morphological aspects. Mayr (1942) further elaborated on this initial concept and declared that
“Species are groups of actually or potentially interbreeding natural populations which are
reproductively isolated from other such groups”.
Dobzhansky (1970), once a more detailed knowledge of inheritance and DNA became available,
further elaborated on the BSC by stating that “Species are … systems of populations; the gene

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exchange between these systems is limited or prevented in nature by a reproductive isolating
mechanism or perhaps by a combination of several such mechanisms”.
White (1978a) accepted the general definition but pointed out emphatically that a species was “at
the same time a reproductive community, a gene pool and a genetic system”.
All of these, and many other, criticisms and comments make up what is the original BSC
concept:
a) Species are defined by distinctness rather than by differences.
b) Species consist of populations rather than unconnected individuals.
c) Species are not defined by the fertility of individuals but by the reproductive isolation of
populations.
d) Species are reproductive communities in which individuals of animal species recognize
potential mates for reproduction.
e) The species is an ecological unit that, regardless of the individuals composing it, interacts as
a unit with other species with which it shares the environment.
f) The species is a genetic unit, a gene pool, whereas the individual is a temporary vessel
holding a portion of the gene pool for a short period of time.
As can be easily seen, this concept of species only applies to sexually reproducing species and
has no applicability to asexually, parthenogenetic or clonally reproducing organisms.
The BSC was often attacked for the difficulty of applying the concept for taxonomical purposes,
both on living species and on fossil species, where, not surprisingly, it would be impossible to
determine whether two fossil organisms could have bred with each other and produced viable
offspring.
Other attacks to the BSC were grounded in the intrinsical non-testability of it for temporally
separated species (such as fossils and current species) and the determination of what degree of
non-viability of hybrids would be sufficient to determine species status; especially since many
hybrids of closely related species are not completely sterile (Sokal and Crovello 1970).
Paterson (1985) and Templeton (1987,1989) attacked the BSC on the grounds that it was a
negative concept involving the formation of isolating mechanisms which they argued were the
product of isolation in the first place rather than the cause of the isolation itself. Paterson
specifically asserted that sterility could only be acquired as an accidental consequence of other
changes. Both these criticisms were countered and shown to be misguided by King (1993).
1.2.1.3. Biological Species Concept (BSC) II – (Mayr 1982)
In response to the multiple criticisms that had been raised at the BSC as first iterated, Mayr
(1982) presented a more detailed and descriptive definition of biological species to be added to
the BSC which was the following: “A species is a reproductive community of populations
(reproductively isolated from others) that occupies a specific niche in nature”.
While seemingly addressing some of the perceived shortfalls of the BSC in his 1982 publication,
namely the inclusion of asexual species, the inclusion of new, and potentially nebulous concepts,
made this new definition rife with unquantifiable parameters which made it difficult to define and
defend.
Hengeveld (1988) attacked this modified BSC concept on the following four areas of weakness:

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a) The concept of niche in ecology is typological, and on the basis of Mayr’s own views on
typological evidence, this should not be used.
b) There are fundamental problems in defining the concepts of “niche” and “population”.
c) Since processes operate on different spatio-temporal scales, clear cut ecological
discontinuities cannot be drawn between species.
d) Including the concept of “niche” in species definitions would restrict such definitions to animal
species only.
As a result of these criticisms, and other similar ones, the revised BSC II concept has enjoyed
little approval and hasn’t become an accepted and used definition of species.
1.2.1.4. The recognition species concept – (Paterson 1978, 1985)
In 1978 Paterson put forth a highly contentious view of species which garnered limited support
and was proven to have an excessive number of inconsistencies to make it of any practical utility
but is interesting to look at for the potential implications of the proposed mechanism and how it
can be applied to the reinforcement scenarios that are the subject of this publication.
Paterson’s model is based on the fertilization mechanisms in place for biparental organisms (and
is therefore not applicable to asexual species) and focuses on the interactions between mating
partners. The essential features, as summarized by King (1993) are the following:
a) The members of a species share a specific mate recognition system (SMRS) to ensure
effective syngamy within a population of organisms occupying their preferred habitat.
b) The characters of the SMRS are adapted to function effectively in this preferred habitat.
c) A new species arises when all members of a small, isolated subpopulation of a parental
species have acquired a new SMRS. This facilitates syngamy under the new conditions and
makes effective signaling impossible between daughter and parental populations. Thus
speciation is the incidental consequence of adaptation to the new environment.
The SMRS as proposed by Paterson includes any gene or genetically controlled character that is
instrumental in the choice of a mate, from signaling and pheromones all the way to physical or
biochemical characteristics of the reproductive organs.
Paterson (1985) then described a species as “the most inclusive population of biparental
organisms which share a common fertilization system”. King (1993) pointed out that this
definition automatically describes a fertilization system that determines:
a) The limits of gene exchange.
b) That members of a species mate positively assortatively through the functioning of their
SMRS.
c) That effective syngamy occurs within a population of a species occupying a preferred habitat
and is ensured by the SMRS.
d) That limits to the field of gene recombination exist.
The criticism to this concept was vast and rapidly expressed. Butlin (1987) pointed out to the
obvious fact that, two species that can mate and produce sterile hybrids (such as Horses and
Donkeys, as per Zong and Fan, 1989) would be considered the same species, thus rendering
the recognition species concept inviable. He then proceeded to state that “species should be
defined by the absence of gene flow, whatever the characters responsible for its prevention”.

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Paterson’s model furthermore would consider polypoid plants, which represent one of the most
accepted methods of instant speciation in plants, as “conspecific since reproductive isolation
between them and their direct ancestor is sometimes not complete” (King 1993). Furthermore,
“A large proportion of the plant kingdom and a number of animal species currently regarded as
good biological and taxonomic species would (…) be regarded as conspecific (…) under
Paterson’s definition” (King 1993).
If applied, the recognition species concept would imply that all species that are capable of
producing sterile F1 hybrids, either in the lab or in the wild, would have to be considered as
being the same species. This would result in creating havoc within the taxonomic world and not
bringing any real advantage in biological terms (after all, there seems to be no practical point in
considering donkeys and horses, or tigers and lions, as representatives of the same species
purely based on the fact that they can generate sterile F1 hybrids).
1.2.1.5. The cohesion species concept – (Templeton 1989)
Templeton (1989) contended that, for the definition of a species and the process of speciation,
isolation was not necessary given it is a “negative phenomenon that could not be selected for”
(King 1993). He suggested to focus attention on the pre-mating reproduction-facilitating
mechanisms and argued that the isolation factor could arise as a byproduct of other
reproductive functions, and that isolation, by and large, was not an active part of speciation. As
a result, he believed that isolating mechanisms were a misleading way of thinking about the
process of speciation. Templeton (1989) agreed in principle with Paterson (1978, 1985) on the
recognition species concept and tried to expand on Paterson’s work to respond to the multiple
criticisms it had been subjected to.
Templeton therefore defined a species as “the most inclusive population of individuals having
the potential for phenotypic cohesion through intrinsic cohesion mechanisms”.
This concept was based on the BSC, the recognition concept and the evolutionary concepts of
species while transferring the focus from isolation mechanisms to cohesion mechanism (King
1993).
Templeton believed that two types of cohesion mechanism were at work, namely genetic
exchangeability (factors that limit the spread of variants through gene flow) and demographic
exchangeability (factors that define the fundamental niche and determine the limits of spread of
the new genetic variants through genetic drift and natural selection).
Templeton, as summarized by King (1993), believed that this new concept provided the
following advantages over the BSC and the recognition concepts:
a) A range of cohesion mechanisms define a species, rather than gene flow which is the major
component of the alternative models.
b) The cohesion concept can be applied to a range of organisms which have diverse
reproductive strategies and lifestyles.
c) A ‘good’ species could be defined as one with distinct levels of genetic and demographic
exchangeability. Templeton regarded this as an important point since the boundaries
defined by genetic and demographic exchangeability are different, and the other species
concepts only recognize the former of these.
d) The cohesion concept clarifies the evolutionary significance of sympatric models of
speciation, for the evolution of demographic non-exchangeability triggers the speciation
process.

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e) Since a broad set of “micro-evolutionary” processes are involved in a species definition,
natural selection can be dealt with as a general principle rather than by having to refer to the
effects on gene flow.
This view was rapidly criticized by Endler (1989) who attacked the idea that gene flow holds
species together by homogenizing allele frequencies and co-adapted gene complexes, claiming
that such mechanisms had been disproven by the isolation by distance concept and the fact
that homogenization only happens for selectively neutral alleles. He also found the concept to
be operationally non applicable and at risk of degenerating into a phenetic species concept.
King (1993) added further criticism to it by describing it as “purely an optimistic rewriting of the
BSC, with an emphasis on those factors which hold a species together rather than those which
isolate it from the next.(…)There seems to be no worthwhile difference between this concept
and that of the biological species”.
1.2.1.6. The Evolutionary species concept by Simpson – (Simpson 1961)
In 1961 Simpson proposed an evolutionary species concept to deal with the impossibility of the
BSC of being applied to temporally sequential species or uniparental organisms. It was
originally a paleontological concept which however was then dramatically and radically altered
in its scope and validity. Simpson (1961) stated that “Species do evolve, and almost always do
so gradually. Among evolutionary species there cannot possibly be a general dichotomy
between free interbreeding and no interbreeding. Every intermediate stage occurs, and there is
no practically definable point in time when two intraspecific populations suddenly become
separate species”.
Feeling the need for a variation of the BSC that could be applied to the fossil record, Simpson
(1961) proposed the following definition of a species:
“An evolutionary species is a lineage (an ancestor-descendant sequence of populations),
evolving separately from others and with its own unitary evolutionary role and tendencies”
King (1993) noted how this concept viewed species as temporal lineages, the constituents of
which changed with time, with the result that a name could be given to a phenotypically distinct
form within a lineage and a different name could be given to a subsequent form in the same
lineage at a later time. These “successive species” would therefore be a direct reflection of
phyletic evolution, an approach that has not been accepted by today’s phylogeneticists, who
regard speciation as a dichotomous event.
Simpson believed that an any point in time there would be a correspondence between BSC
species concepts and evolutionary species concepts in biparental organisms, due to the fact
that biological species reflect morphological divergence between lineages at any one time.
In addition to this view, the evolutionary concept also allowed the possibility for two species to
interbreed without losing their evolutionary roles, as long as the amount of interbreeding was
not sufficient to “cause their roles to merge”.
Mayr (1982) criticized Simpson’s concept of species on two levels, the first being that it can be
considered simply a typological description which would completely ignore cryptic and polytypic
species and the second one being that he viewed this model as prone to minimize the role of
factors that cause and maintain discontinuities between species and concentrate exclusively on
how to delimit multidimensional species taxa.
In addition to these two major critics he also was skeptical of the incorporation of a “unitary
evolutionary role” into the definition of a species, given that this role is an unmeasurable

Page 15 of 177
character. This point was similar to the criticism that Hengeveld (1988) raised of the “niche”
concept that Mayr had incorporated into his own revised BSC concept.
King (1993) noted Mayr’s criticisms but pointed out how the fundamental criticism was “that of
multiple species occurring in a simple non-branching lineage”.
Figure 1.2.1.6. – a) a lineage of biological species showing that speciation is accompanied by a
dichotomous branching event. b) the evolutionary species concept in Simpson’s (1961) terms,
suggested that a single lineage could change from species to species through geological time.
(From King 1993, fig. 2.2., pg. 20)
Sokal and Crovello (1970) summarized the concept of the evolutionary species as presented by
Simpson (1961) as “so vague as to make any attempt at operational definition foredoomed to
failure”.
1.2.1.7. The Evolutionary species concept by Wiley– (Wiley 1978)
Seeing the potential shortfalls of Simpson’s model, Wiley (1978) proposed a modified
evolutionary species concept which he defined as:
“A species is a single lineage of ancestral descendant populations of organisms which
maintains its identity from other such lineages and which has its own evolutionary tendencies
and historical fate.”
Corollaries and implications of this model were that:
a) All organisms, past and present, belong to some evolutionary species
b) Separate evolutionary lineages (species) must be reproductively isolated from one another
to the extent that this is required for maintaining their separate identities, tendencies and
historical fates.
c) The evolutionary species concept does not demand that there be morphological or phenetic
differences between species, nor does it preclude such differences.

Page 16 of 177
d) No presumed separate, single evolutionary lineage may be subdivided into a series of
separate ancestral and descendant species.
Wiley, as Simpson (1961) before, contended that the evolutionary species concept also
included asexually reproducing organisms.
The major differences from the Simpson (1961) concept were that no species could be divided
in ancestral and descendant species and that the Wiley model didn’t require morphological or
phenetic differences between species (thus accounting for cryptic and sister species). He also
removed the “unitary evolutionary role” definition that was criticized in the Simpson (1961)
model.
King (1993) analyzed this species concept and pointed out to the following improvements over
the Simpson (1961) model:
a) It implies that the species is the most inclusive unit of evolution.
b) It does not imply that species must change; a species “maintains its identity” rather than
“evolves”.
c) “Identity” in the context of this definition means individual identity and does not infer either
stasis or change in morphology.
d) Species are thought of as individuals rather than classes.
e) Species are historical, temporal and spatial entities.
f) Whether a group of organisms is or not a species becomes an hypothesis to be tested.
Evidence which can be used to test this proposition is derived from genetic, phenetic,
spatial, temporal, ecological, biochemical and/or behavioral sources.
He, however, criticized the model in as much as it created nomenclatorial problems since
“Naming morphologically indistinguishable species, could not only lead to taxonomic mayhem,
but could also further erode the correspondence between biological and evolutionary species”.
Further criticism was levied by Hecht (1983) and Hecht and Hoffman (1986) who claimed that
no single criteria from the Wiley (1978) model could be used unequivocally, and stated that the
idea that morphospecies approximate actual biological species is without foundation.
Mayr (1982) also attacked the typological approach preferred by Wiley and other cladists on the
grounds that “The principal weakness of the so-called evolutionary species definitions is that
they minimize (if not ignore) the crucial species problem, the causation and maintenance of
discontinuities between species, and concentrate instead on the problem of how to delimit
multidimensional species taxa. Yet they do not even meet the limited objective of how to delimit
such open-ended systems.”.
1.2.1.8. The Ecological species concept – (Van Halen 1976)
Van Halen (1976) also proposed a variation on the ecological species concept as a result of
discordances he perceived between the BSC and apparent speciation mechanisms observed in
American oak trees (genus Quercus).
Van Halen (1976) proposed a self-described “radical” change to the Simpson (1961) model to fit
his needs for classification of the American oak trees. His approach was based on the following
three central principles:
a) Genes are of minor importance in evolution and should only be considered as molecules.
b) The control of evolution is ecological and under the constraints of individual development.

Page 17 of 177
c) Selection acts primarily on genotypes.
As a consequence, Van Halen (1976) defined a species as:
“A lineage (or a closely related set of lineages) which occupies an adaptive zone minimally
different from that of any other lineage in its range and which evolves separately from all
lineages outside its range.”
He also further added the following corollaries:
a) A population was a group of individuals in which adjacent individuals at least occasionally
exchanged genes reproductively and did so more frequently than with individuals outside
the population.
b) Lineages were closely related if they had occupied the “adaptive zone” since their latest
common ancestor. If that zone had changed, they were closely related if new adaptations
had been transferred among lineages rather than originating separately in each.
c) An “adaptive zone” was some part of the resource space together with whatever predation
and parasitism occurred on the group considered. It was part of the environment and
existed independently of any inhabitants it might have.
d) “Range” was both geographic and temporal.
e) The “occupation” of an adaptive zone was a difference in population density; a species
could occupy more than one adaptive zone.
f) Reproductive isolation was of minor evolutionary importance and needed little consideration.
This concept was rapidly criticized by Wiley (1978) on the basis that species do not have to
occupy minimally different niches or adaptive zones from other species to be regarded as
species (i.e. two species can occupy the same niche) and on the fact that Van Halen’s definition
allowed to argue that a species forced into extinction in a particular habitat due to interspecific
competition wasn’t really a species at all.
King (1993) further extended the criticism and pointed out that Van Halen’s view of species was
predicated on characteristics such as “adaptive zone” and “range” that were difficult to quantify
and define and, as a result, his definition of species would “appear to be largely unworkable”.
He also noted how “Van Halen’s ideas on the significance of genic change and reproductive
isolation appear to be unorthodox”.
1.2.1.9. The Phylogenetic species concept – (Cracraft 1983)
Cracraft (1983) believed that the BSC failed to resolve the pattern and process of taxonomical
differentiation and disagreed with the BSC’s focus on reproductive isolation and therefore
proposed his own Phylogenetic species concept.
Cracraft viewed reproductive isolation as a secondary aspect and focused his attention on
taxonomic differentiation. He argued that phenotypes are not necessarily morphological but may
also include recognizable biochemical, physiological or behavioral attributes that allow
differentiation and prevent, by their intrinsical nature, interbreeding with other taxa.
These taxonomic units may be equivalent to biological species in some cases but only when
species are monotypic, while he believed that, in the majority of cases, biological species would
contain two or more evolutionary taxonomic units.
In order to mitigate the possible confusion of this unintended consequence of the phylogenetic
species concept, Cracraft proposed that a species should be defined from the perspective of the
results of evolution, rather than the processes that produce those results.

Page 18 of 177
He therefore proposed his definition of species as follows:
“A species is the smallest diagnosable cluster of individual organisms within which there is a
parental pattern of ancestry and descent.”
He then proceeded to present the following corollaries to explain and define boundaries for the
phylogenetic concept of species:
a) Although most species would be defined by uniquely derived characters, these cannot be
included in the species definition, since it would not be possible to recognize ancestral
species.
b) Species must be diagnosable from all other species.
c) Diagnostic characters must be passed from generation to generation and must be taken do
define a reproductive community.
d) A species definition must have some notion of reproductive cohesion, of parental ancestry
and descent, although this is not predicated on reproductive disjunction.
King (1993) analyzed Cracraft’ position and noticed how it eliminated any reference to
reproductive isolation from other species-level taxa and how species were recognized simply in
terms of their status as diagnosable evolutionary taxa. This allowed two sister taxa to hybridize
broadly and still be considered as species if each was diagnosable as a discrete taxon. He
further proceeded to point out that the fundamental weakness of this model is the limit to which
the fact of accepting any character as being suitable for diagnosis, rather than solely limiting the
characters to morphological ones, and the workability of species defined by such terms.
He proposed the case of chromosomal races within a morphologically indistinguishable species
range which would be recognized as independent species by the Phylogenetic Species concept
as proposed by Cracraft. While this level of species definition would still be potentially
acceptable, further differences such as subpopulations of electrophoretically distinct groups
would also be considered species, as would be discrete mtDNA lineages within these
electrophoretically distinct groups and so on until the level of individual alleles has been
reached.
It is clear how taking the Cracraft definition as proposed would lead to excessive fragmentation
of species into increasingly small groups with very little or no taxonomical value associated with
them.
King (1993) highlighted how “one of the great problems associated with the phylogenetic
species approach is the inconsistency which it creates within morphologically recognizable
species.(…) The phylogenetic species concept has the potential to create an enormous
imbalance between taxa, if each of the detected entities are to be recognized”. King argued that
well-known species, which have been characterized genetically to a much broader extent than
little-known or studied species, would end up being subdivided in several phylogenetic species
which would not be representative of real differences in variability between the well-known and
the little-known species, but simply reflective of the disproportionate amount of sequencing that
the former have had performed on them, compared to the latter.
1.2.1.10. Species concept as used in this publication
By quickly reviewing the major species definitions presented above, it becomes rapidly clear
how the evolutionary species concepts presented appear to have very limited practical use and
applicability (King 1993), being extremely specialized and based on very vague and non-
descript concepts and definitions.

Page 19 of 177
In order for a species concept to be viable it must meet two basic criteria, the first one being the
capability of placing a name on an animal or plant species that is encountered, in a way that will
satisfy the scientific community in general.
The second criteria is that this species concept be capable of satisfying the very different needs
of the scientific community.
The latter of the two requirements is indeed the most problematic, since the needs of
paleontologists, systematists, ecologists, geneticists and molecular biologists are very different
and sometimes at odds with each other.
These differences aren’t simply based on different views of what a species is, but are more
deeply rooted in the techniques and aspects of biology that each group of scientists focuses on.
This dichotomy between biological and evolutionary species concepts reflects this basic divide
between the BSC concept, which focuses on living, testable populations, and species concepts
that apply to extinct or fossil species for which the BSC model has little application.
This publication, given it is focused on the role of chromosome change in speciation, will take,
by and large, the BSC concept, specifically extended to become Chromosomal speciation, as
the overall concept of species to be utilized.
In doing this we are following the view expressed by King (1993) as: “Since chromosomal
speciation is one of the major modes of speciation and it is based on reproductive isolation, the
only possibility is to recognize a species definition incorporating this process, i.e. the BSC.”.
The view that will be investigated in this publication is that of the fixation of negatively heterotic
structural chromosomal rearrangements which can effectively act as post-mating isolating
mechanism by preventing gene flow and enforcing reproductive isolation.
1.2.2. Historical views on chromosomal speciation
Historically speaking, the theory of chromosomal speciation has been both rejected and
recognized as inevitable, often by the same researchers. The best example of this are the
following two quotations from Ernst Mayr, the first from 1963, and the second from 1982, which
show the magnitude in the change of position that occurred in the short span of less than twenty
years:
“There was a widespread belief among early cytogeneticists that chromosomal rearrangement
was the essential step in speciation. Proposed as an alternative to geographic speciation, the
chromosomal speciation hypothesis is not valid.” Mayr (1963)
“The fact of chromosomal speciation poses a problem” Mayr (1982)
This confusion appears to derive from two different factors, the first being the ill-conceived
assumption that chromosomal rearrangements are a conditio sine qua non for speciation, which
is clearly incorrect, given that there are numerous examples of species that have speciated
without any significant change in chromosome morphology (King 1993). These cases are
examples of speciation via allopatric mechanisms and are well exemplified in several
Drosophila species from Hawaii (Carson et al. 1967).
The second factor, which is by and far the most relevant, is that the critics of the theory of
chromosomal speciation have failed to differentiate between neutral or positively heterotic

Page 20 of 177
chromosomal rearrangements, which have the potential to be present as polymorphisms in
Hardy-Weinberg equilibrium within populations, and negatively heterotic chromosomal
rearrangements which cannot do so (see results and discussion sections).
The latter category will either inevitably be eradicated from the gene pool or, in very select
conditions, will evolve into the first step of a post-mating reproductive barrier that will then either
reinforce to pre-mating barriers (via reinforcement mechanisms) and speciate, or end up being
reabsorbed into the original population and disappear from the genetic record.
King (1993) stated that “chromosomal polymorphism, chromosomal addition or fixed
chromosomal differences which are neutral” (…)may have had nothing to do with past
cladogenic events”.
Several models of chromosomal speciation have been proposed over the years, starting with
the triad hypothesis of Wallace (1953), the salutatory model of Lewis (1966), quantum
speciation (Grant 1971), stasipatric speciation (White 1978) and multiple subsequent models
based upon founding situations.
White (1978) very clearly stated his position on the preeminence of karyotypic changes as
causal factors in speciation as follows:
“Over 90% (and perhaps 98%) of all speciation events are accompanied by karyotypic
changes and in the majority of these cases, the structural chromosomal rearrangements
have played a primary role in initiating divergence.” (White, 1978, p. 324)
1.2.3. Frequency of chromosomal rearrangements
Chromosomal rearrangements are observed in all types of animals and plants in frequencies that are,
to some extent, dependent on the species observed. For example, Wang et al. (2013) and Abdalla et
al. (2013) report an incidence of Robertsonian translocation in humans of one in 1,000 newborn babies.
O’Neill (2010) gives a combined figure of 0.6% to 1% of newborns carrying Robertsonian
translocations, reciprocal translocations and chromosomal inversions. In humans, by far, chromosomal
inversions appear to be the most common rearrangement in the overall population with an estimated
incidence of 1-3% (Shaw et al. 2004 and Hsu et al. 1987).
White (1978) extended his analysis of chromosomal rearrangement rates to organisms as diverse as
lilies, grasshoppers and humans, and observed a mutation rate for novel chromosomal rearrangements
in the order of 1 in 500 individuals. This data is an overall grouping of multiple kingdoms and types of
rearrangements and should therefore be used simply as an order of magnitude data point.
Lande (1979) studied different rearrangements in various species of Drosophila and obtained an
incidence of reciprocal translocations between 10-4
and 10-3
per gamete per generation.
The variability in the rate was due to having used several Drosophila species that presented
translocation incidences as low as 2 in 5600 for wild populations of D. ananassae (Yamaguchi et al.
1976) and as high as 1 in 531 for wild strains of D. melanogaster (Berg, 1941).
Spontaneous chromosome fusions are reported as being more frequent, with the chromosome fusion
of chromosome 21 that produces Down syndrome in humans estimated to occur at a rate of 3x10-5
per
gamete per generation (Hamerton, 1971).
Lande (1979) also reported that fusions of the smaller chromosomes in man occurred at a rate of 10-4
per individual while pericentric inversions occurred at 0.4 x 10-4
.
Yamaguchi (1976) observed a rate of pericentric inversions in D. melanogaster of 3 x 10-3
in laboratory
strains (this rate might have been increased by the presence of transposable elements in the laboratory
lines).

Page 21 of 177
King (1983) detected pericentric inversions and chromosome fusions in wild populations of gekkonid
lizards of the Gehyra australis, G. pilbara and G. variegata-punctuata complexes varying between 1 in
6 and 1 in 41 (average 1 in 24 for 337 specimens).
Given that the data were measured by sampling wild populations and on adult individuals, it is possible
that some of the changes, particularly the inversions, were in fact polymorphisms and not neo-
mutations.
Jacobs et al. (1992) calculated chromosome abnormalities in newborn humans to be between 0.6%
and 0.92% showing 112 rearrangements (32 balanced and 80 unbalanced) over more than 14,000
samples collected between 1976 and 1990.
Rates of mutation in plants are even higher, with data that points to incidences as high as 1 in 50 for
the dioecious angiosperm Rumex acetosa (Parker et al. 1988). Within the specimens that Parker
analyzed it is interesting to note how the rate of mutation is two orders of magnitude higher in the Y
chromosomes than it is in the autosomes.
Parker et al. (1988) also noted the high mutation rate in the polytypic Scilla autumnalis where 5% to
10% of the sampled adult plants showed unique chromosomal rearrangements (mostly centromeric
shifts).
OBSERVED RATES OF CHROMOSOMAL REARRANGEMENTS: WITHIN SPECIES
Species Type Incidence Authority
Homo sapiens sapiens Robertsonian
Translocation (RBT)
1:1,000
(0.1 %)
Wang et al. (2013) and
Abdalla et al. (2013)
Homo sapiens sapiens RBT, balanced
translocations,
inversions
6:1,000 to 1:100
(0.6% to 1%)
O’Neill (2010)
Homo sapiens sapiens Chromosomal
inversions
1:100 to 3:100
(1% to 3%)
Shaw et al. (2004)
and
Hsu et al. (1987)
Homo sapiens sapiens Fusion of
chromosome 21
(Down syndrome)
3x10-5
per gamete per
generation
(0.003%)
Hamerton (1971)
Homo sapiens sapiens Fusions of smaller
chromosomes
10-4
per individual
(0.01%)
Lande (1979)
Homo sapiens sapiens Pericentric inversions 0.4 x 10-4
per individual
(0.004%)
Lande (1979)
Homo sapiens sapiens Various, balanced
and unbalanced
112:14,667 Jacobs et al. (1992)

Page 22 of 177
(0.7631%)
Homo sapiens sapiens Various, balanced 32:14,667
(0.218%)
Jacobs et al. (1992)
Homo sapiens sapiens Various, unbalanced 80:14,667
(0.5451%)
Homo sapiens sapiens Reciprocal
translocations
39:14,667
(0.2657%)
Various Multiple types 1:500
(0.2%)
White (1978)
Drosophila (various) Reciprocal
translocations
10-4
to 10-3
per gamete
per generation
(0.01% to 0.1%)
Lande (1979)
Drosophila ananassae Reciprocal
translocations
2:5,600
(0.0357%)
Yamaguchi et al.
(1976)
Drosophila melanogaster
(wild strains)
Reciprocal
translocations
1:531
(0.188%)
Berg (1941)
Drosophila melanogaster
(laboratory strains)
Pericentric inversions 3 x 10-3
(0.3%)
Yamaguchi (1976)
Gekkonid lizards of the
Gehyra australis, G.
pilbara and G. variegata-
punctuata complexes
Pericentric inversions 1:24
(4.166%)
King (1983)
Rumex acetosa Multiple types 1:50
(2%)
Parker et al. (1988)
Scilla autumnalis Multiple unique
chromosomal
rearrangements
(mostly centromeric
shifts)
1:20 to 1:10
(5% to 10%)
Parker et al. (1988)
Studies of naturally occurring or laboratory produced inter-species hybrids have shown extraordinarily
high rates of mutation. Shaw et al. (1983) detected both increased mutation rates and numerous
simultaneous mutations occurring within hybrid-backcross progeny in Caledia captiva.

Page 23 of 177
Similar data was reported for Atractomorpha similis hybrids by Peters (1982). Hagele (1984) also
measured the same effects in crosses between Chironomus thummi thummi and Chironomus thummi
piger where breaks in salivary gland chromosomes were present in 3% to 79% of nuclei.
Similarly, Naveira and Fontedvila (1985) observed comparable incidences and found a 30 times
greater rate of chromosomal mutation in hybrid males compared to hybrid females in crosses of
Drosophila serido with Drosophila buzzatii.
All these experimental data point out to the fact that chromosomal rearrangements are a fairly frequent
event and that they are often produced in very high rates in hybrid zones, thus representing a good
candidate for increased speciation likelihood (King 1993).
1.2.3.1. Types of negatively heterotic chromosomal rearrangements
Chromosomal rearrangements are generally divided into the following main categories:
Type of rearrangement Negatively heterotic
Deletion Potentially, depending on nature of lost portion
(gene effects)
Insertion Potentially, depending on nature of
duplicated/inserted portion (gene effects)
Reciprocal Translocations Strongly negatively heterotic in heterozygotes.
Neutral in homozygotes.
Tandem Fusion Negatively heterotic.
Robertsonian Fusion Potentially negatively heterotic, dependent on
specific fusion/translocation.
X-Autosome translocations Potentially negatively heterotic, dependent on
specific fusion/translocation. Compounded by
X inactivation effects (Haldane’s rule).
X-Autosome fusions Potentially negatively heterotic, dependent on
specific fusion/translocation. Compounded by
X inactivation effects (Haldane’s rule).
Pericentric Inversions Minor negatively heterotic effects. Often
polymorphic. Mechanisms of chiasmata
suppression often noted.
Paracentric Inversions Minor negatively heterotic effects. Often
polymorphic. Mechanisms of chiasmata
suppression often noted.
Heterochromatin additions Generally no negatively heterotic effects.
Often polymorphic.

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Of the above list, the rearrangements that have potential speciation roles (King 1993) are the
Tandem fusions, the Robertsonian fusions, the balanced reciprocal translocations, the X-
autosome fusions and translocations and certain specific cases of inversions (both pericentric
and paracentric).
For the purposes of this work, the focus will be exclusively on balanced reciprocal translocations
and their role in speciation, for which detailed computer modeling will be presented.
1.2.3.2. Fertility effects of balanced chromosomal translocations on carriers
In the case of balanced reciprocal translocations, heterozygosity will generally result in the
production of chromosomal multivalents (chain or ring) at metaphase which segregate to
produce 50% euploid and 50% aneuploid gametes (see figure 1.2.3.2.a. redrawn from King
1993 and John and Freeman 1975).
White (1973) observed how such a high level of aneuploidy results in the production of unviable
or lethal gametes. Cleland (1962) reported, however, cases in plants where multiple
translocations formed rings at anaphase, reducing the effects on segregation. These patterns,
however, seem to be more the exception rather than the rule as, by and large, most
translocations show the deleterious effects reported by White (1973).
Figure 1.2.3.2.a. – Structural heterozygosity for a single reciprocal translocation can lead to the
formation of both balanced and unbalanced gametes, depending on the form and orientation of
multivalents at meiosis. (Redrawn from King 1993, fig. 5.3., pg. 78 and from John, 1976)
The outcome of the meiotic process depends on how the multivalents orient, which is a
stochastic phenomenon, and therefore each possible gamete is represented in equal
proportions.

Page 25 of 177
The effects of these unbalanced gametes are only seen in the heterozygote, given the
homozygote presents a homogenous chromosomal complement which segregates normally,
producing a full set of balanced, and structurally identical, gametes.
The effect on the fertility for the heterozygote is not only intrinsical to the way the gametes
segregate, but also dependent on whether the individual will mate with a homozygote (either
translocated or wild type) or another heterozygote.
Figure 1.2.3.2.b. – Types of gametes produced by Wild Type (non-translocated), translocated
heterozygotes and translocated homozygotes.
If we look at the different gametes produced by the homozygotes and the heterozygotes (as
summarized in figure 1.2.3.2.b.) we see how the heterozygote gives origin to six different types
of gametes, present in different proportions, half of which are balanced and half unbalanced.
In order to determine the possible fertility effects we need to prepare a mating table for the
possible crosses and calculate the probability and outcomes (balanced/unbalanced) of each
mating. The following mating tables present the results of the possible matings (we indicate the
non-Translocated as WT, the heterozygote as M1 and the homozygote as NS):

Page 26 of 177
WT X NS cross
Wild
Type
(WT)
Translocated
Homozygote
(NS)
Resulting
Chromosomal
Asset
Balanced
(Y/N)
Resulting
genotype
Viable
fraction
of
possible
matings
Gametes ABCD BCAD ABCD/BCAD Y M1 100%
Overall cross viability 1
WT X WT cross
Wild
Type
(WT)
Wild
Type
(WT)
Resulting
Chromosomal
Asset
Balanced
(Y/N)
Resulting
genotype
Viable
fraction of
possible
matings
Gametes ABCD ABCD ABCD/ABCD Y WT 100%
NS X NS cross
Translocated
Homozygote
(NS)
Translocated
Homozygote
(NS)
Resulting
Chromosomal
Asset
Balanced
(Y/N)
Resulting
genotype
Viable
fraction
of
possible
matings
Gametes BCAD BCAD BCAD/BCAD Y NS 100%
WT X M1 cross
Wild Type
(WT)
Translocated
Heterozygote
(M1)
Resulting
Chromosomal
Asset
Balanced
(Y/N)
Resulting
genotype
Viable
fraction of
possible
matings
Gametes ABCD ABCD ABCD/ABCD Y WT 1/4
Gametes ABCD BCAD ABCD/BCAD Y M1 1/4

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Gametes ABCD ABAD ABCD/ABAD N None 0
Gametes ABCD BCCD ABCD/BCCD N None 0
Gametes ABCD ABBC ABCD/ABBC N None 0
Gametes ABCD CDAD ABCD/CDAD N None 0
Overall cross viability 1/2
NS x M1 Cross
Translocated
Homozygote
(NS)
Translocated
Heterozygote
(M1)
Resulting
Chromosomal
Asset
Balanced
(Y/N)
Resulting
genotype
Viable
fraction
of
possible
matings
Gametes BCAD ABCD BCAD/ABCD Y WT 1/4
Gametes BCAD BCAD BCAD/BCAD Y M1 1/4
Gametes BCAD ABAD BCAD/ABAD N None 0
Gametes BCAD BCCD BCAD/BCCD N None 0
Gametes BCAD ABBC BCAD/ABBC N None 0
Gametes BCAD CDAD BCAD/CDAD N None 0
M1 x M1 Cross
Translocated
Heterozygote
(M1)
Translocated
Heterozygote
(M1)
Resulting
Chromosomal
Asset
Balanced
(Y/N)
Resulting
genotype
Viable
fraction
of
possible
matings
Gametes ABCD ABCD ABCD/ABCD Y WT 1/16
Gametes ABCD BCAD ABCD/BCAD Y M1 1/16
Gametes ABCD ABAD ABCD/ABAD N None 0
Gametes ABCD BCCD ABCD/BCCD N None 0
Gametes ABCD ABBC ABCD/ABBC N None 0
Gametes ABCD CDAD ABCD/CDAD N None 0
Gametes BCAD ABCD BCAD/ABCD Y M1 1/16
Gametes BCAD BCAD BCAD/BCAD Y NS 1/16
Gametes BCAD ABAD BCAD/ABAD N None 0
Gametes BCAD BCCD BCAD/BCCD N None 0
Gametes BCAD ABBC BCAD/ABBC N None 0
Gametes BCAD CDAD BCAD/CDAD N None 0
Gametes ABAD ABCD ABAD/ABCD N None 0

Page 28 of 177
Gametes ABAD BCAD ABAD/BCAD N None 0
Gametes ABAD ABAD ABAD/ABAD N None 0
Gametes ABAD BCCD ABAD/BCCD Y M1 1/64
Gametes ABAD ABBC ABAD/ABBC N None 0
Gametes ABAD CDAD ABAD/CDAD N None 0
Gametes BCCD ABCD BCCD/ABCD N None 0
Gametes BCCD BCAD BCCD/BCAD N None 0
Gametes BCCD ABAD BCCD/ABAD Y M1 1/64
Gametes BCCD BCCD BCCD/BCCD N None 0
Gametes BCCD ABBC BCCD/ABBC N None 0
Gametes BCCD CDAD BCCD/CDAD N None 0
Gametes ABBC ABCD ABBC/ABCD N None 0
Gametes ABBC BCAD ABBC/BCAD N None 0
Gametes ABBC ABAD ABBC/ABAD N None 0
Gametes ABBC BCCD ABBC/BCCD N None 0
Gametes ABBC ABBC ABBC/ABBC N None 0
Gametes ABBC CDAD ABBC/CDAD Y M1 1/64
Gametes CDAD ABCD CDAD/ABCD N None
Gametes CDAD BCAD CDAD/BCAD N None
Gametes CDAD ABAD CDAD/ABAD N None
Gametes CDAD BCCD CDAD/BCCD N None
Gametes CDAD ABBC CDAD/ABBC Y M1 1/64
Gametes CDAD CDAD CDAD/CDAD N None
We can see from the above mating tables how there is no adverse fertility effect in matings
between homozygotes, there is a reduction to ½ fitness in matings between homozygotes
(either WT or NS) and heterozygotes and a dramatic decrease in viability to 5/16 for crosses
among M1 heterozygotes.
It is worthy of note to point out to how the effect on the fitness of M1xM1 crosses is mitigated by
the chance possibility of unbalanced gametes balancing each other out (in absence of this
factor the expected fitness would be even lower, at 1/4).
The following table summarizes this data and the resulting genotypes:
CROSSES Fitness Resulting genotypes
Combined values
(fitness x fraction)
WT WT 1 WT WT
NS NS 1 NS NS
M1 M1 1/2 1/2 WT + 1/2 M1 1/4 WT + 1/4 M1
M1 WT 1/2 1/2 M1 + 1/2 NS 1/4 M1 + 1/4 NS
M1 M1 5/16 3/5 M1 + 1/5 NS+1/5 WT 3/16 M1 + 1/16 NS + 1/16 WT
WT NS 1 M1 M1
We shall examine the effects of these differential fitnesses in the materials and methods and the
discussion sections.

Page 29 of 177
1.2.4. Chromosomal differences between closely related species in nature and among
domesticated animals
Closely related species are known for presenting both a very high level of genetic similarity (which can
be higher than 99% or more of genetic loci) while often presenting chromosomal differences that are
immediately evident.
Varki and Altheide (2005) reported on the similarities between the Chimpanzee (Pan troglodytes) and
Human (Homo sapiens sapiens) genomes and observed a higher genetic difference than initially
expected (initial estimates were expected to show a difference of approximately 1% of the genome but
sequencing provided a corrected value at 4%). Multiple inversions and rearrangements were also
detected by other authorities (Yunis et al. 1980; Yunis and Prakash 1982; Nickerson and Nelson 1998;
Fan et al. 2002a,b; Dennehey et al. 2004) and several new smaller chromosomal regions containing
likely inversions and rearrangements were highlighted by The Chimpanzee Sequencing and Analysis
Consortium (2005) as well as by Newman et al. (2005).
Newman et al. (2005) also reported 15 inversion events larger than 20 Mb (large enough to be
considered proper inversions and not inverted duplications) between chimpanzee and human
genomes, and Stankiewwicz et al. (2001) identified a 4:19 translocation between human genome and
gorilla genome (Gorilla gorilla).
Dutrillaux (1980) noted how human chromosome 2 appears as two separate chromosomes among the
karyotypes of the great apes.
Baker et al. (1985) reports how the South American verpertilionid bats of the Rhogeesa tumida-parvula
complex are known to have seven distinct cytotpes characterized by thirteen different fusions, with two
allopatric samples from Belize and Nicaragua differing by eight chromosomic fusions.
Reig et al. (1980) described six distinct chromosomal forms of Venezuelan Spiny rats of the
Proechimys guairae complex, each corresponding to two recognized species and four subspecies with
were very difficult to differentiate morphologically. The different complements were characterized by
single or multiple Robertsonian rearrangements and pericentric inversions. Genetic differences were as
low as D=0.014 between adjacent species up to D=0.134 between species at the opposite ends of the
linear spatial array (the speciation events appear to have sequentially happened geographically on the
direction bisecting Venezuela along the major mountain axis).
The Rattus rattus complex (King 1993) presents both karyotypically identical allopatric species (such as
R. lutreolus, R. tunneyi and R. fuscipes), which are genetically and morphologically different but can
produce fertile hybrid progeny and are kept separate exclusively via geographic isolation, as well as
sympatric species with massive chromosomal differences between them such as R. sordidus, R. colletti
and R. villosissimus which are reproductively isolated but genetically indistinguishable.
Yosida (1980) reported five separate chromosomal races within the Rattus rattus complex,
characterized by chromosomal fusions and fissions but very limited genetic differences between them.
Notwithstanding the negligible genetic differences, Yosida (1980) reported how laboratory
hybridizations between the different chromosomal races failed to produce live progeny or presented
extremely limited litter sizes.
Wahrman and Gourevitz (1973) reported extensive chromosomal variation in the great sand gerbil
complex, Gerbillus pyramidium, with two separate chromosomal races characterized by seven fixed
chromosome fusions and separated by a 150x150 km hybrid zone where multiple karyotypic forms
were encountered. Nevo (1982) analyzed the closely related G. allenbyi species and found that the
genetic differences between G. pyramidium and G. allenyi were very low (D=0.11) and comparable in
entity to intra-species differences between G. allenyi populations, but chromosomal differences were
sufficiently major to provide complete reproductive isolation between the two species.

Page 30 of 177
The fossorial mole rat Spalax ehrenbergi complex presents four chromosomal races (2n=52, 54, 58
and 60) that are morphologically indistinguishable (Wahrman et al. 1969, Nevo 1985). Nevo and Bar-el
(1976) found that, the larger the chromosome differences that occurred between karyotypes in the wild,
the narrower the hybrid zones were. Wahrman et al. (1985) argued that this was the result of an
ongoing speciation process occurring between chromosomal races and involving reduced hybrid
fitness. Nevo et al. (1972 and 1978) determined genetic difference to be very low between the
chromosome races (D varying from 0.002 to 0.07). Catzeflis et al. (1989) further analyzed the
divergence and measured a 0.2% to 0.6% base pair mismatch between chromosomal races.
King (1979,1984) reported a series of chromosome races in the gekkos of the Gehyra variegate-
punctuata complex which presented high genetic similarity but major chromosomal differences. A total
of 11 different chromosomal races, distributed between G. pilbara, G. minuta, G. nana, G. punctuata
and G. variegata species were observed. Distances between species and chromosomal races went
from virtually undistinguishable (D=0.023) to very similar (D=0.102).
Sites and Davis (1989) confirmed earlier hypotheses of multiple chromosomal races in the Iguanid
lizard complex Sceloporus grammicus and observed the extreme spatial limitation of hybrid zones in
the wild (at times narrower than 500 meters). A total of 8 chromosomal cytotypes were detected, with
genetic differences as low as zero (D=0.00) and fixed chromosomal differences between each one of
them (chromosomal fissions).
King and Rofe (1976) and King and King (1977) subdivided the southern Australian gecko
Pyllodactylus marmoratus in four different chromosomal races characterized by variation between
2n=32 and 2n=36 and allopatrically distributed. Chromosomal races with different numbers differed by
single chromosome fusions while the ones with the same number differed by a characteristic sex
chromosome heteromorphism. King (1993) reported genetic differences between D=0.08 and D=0.18
and detection of a cryptic species characterized by three fixed chromosomal rearrangements.
The genus of pocket gophers Thomomys (King 1993) is characterized by an extreme chromosomal
variability with chromosome numbers varying between 2n=40 and 2n=60. The genus shows extensive
polytypism based on chromosome fusions and pericentric inversions. When species are parapatrically
distributed, chromosomal monomorphy is observed. Hybridization is either absent or present with
hybrid zones of variable width.
The Peromyscus maniculatus deer mice complex (King 1993) is characterized by an assemblage of 65
species that all share the same chromosome number (2n=48) and are differentiated by pericentric
inversions, often present as polymorphisms. Loudenslager (1978) measured the genetic identities from
nine populations of Peromyscus maniculatus nebrascensis that showed chromosomal polymorphisms
and detected limited genetic differences, measured as being between D=0.05 and D=0.07.
The shrews of the Sorex araneus complex have been extensively karyotyped (King 1993, Wojcik 1993)
and shown to have chromosome numbers varying between 2n=20 and 2n=34. These forms are
distinguished by fixed paracentric and pericentric inversions, reciprocal translocations and fusions.
Hauser et al. (1985) measured the mean genetic difference between species at D=0.055 and proposed
that all the eight species had speciated chromosomally. The overall picture for Sorex araneus (King
1993) is further complicated by the presence of intricate chromosomal polymorphisms within species
and broad hybrid zones between chromosome races. Up to 40 different chromosome races have been
described between Western Europe, Eastern Europe and Siberia. King (1993) reports how the
chromosome races of Sorex araneus fail to establish fixed genetic differences, with the only
differences being the chromosomal rearrangements that segregate in local populations.
Amongst the different species of pigs, chromosome fusions are one of the major notable differences.
Species as diverse as the giant forest hog (Hylochoerus menertzhageni), the warthog (Phacochoerus
aethiopicus), the African bush pig (Potamochoerus porcus), the European wild boar (Sus scrofa) and

Page 31 of 177
the domestic pig (Sus scrofa) are chromosomally similar and distinguished by Robertsonian fusions
(Bosma 1978; Melander and Hansen-Melander, 1980). Wild boars are characterized by chromosomal
polymorphisms for two independent fusions producing chromosome numbers of 2n=36, 37 and 38
while domestic pigs are monomorphic.
Over 50 species of Bovoidea (cattle) have been chromosomally characterized (Wurster and
Benirschke, 1968), highlighting substantial interspecific and intergeneric chromosome differences with
numbers varying from 2n=30 to 2n=60. This variation is the result of chromosome fusions, inversions,
reciprocal translocations and tandem fusions.
King (1993) reports how the members of the tribe Caprini (Sheep, goats and their relatives) differ
between themselves by chromosome number variations deriving from Robertsonian fusions, with
chromosome numbers from 2n=48 to 2n=60. Domestic sheep are monotypic (2n=54) but Robertsonian
fusion polymorphisms have been encountered.
1.2.4.1. Examples of hybrid sterility and reduced viability in hybrids
Hybrid sterility and reduced viability has been a well-known and documented phenomenon
since mankind first started crossing donkeys and horses to produce mules and hinnies (which
however has proven to be less clear-cut than what was thought to be the case).
Dobzhansky (1933) first published a detailed study on hybrid sterility in Drosophila
pseudobscura which is still valid today. He stated that “Offspring from interspecific crosses are
frequently equal or superior to their parents in somatic vigor, and are, nevertheless, partially or
completely sterile. The sterility is due to a disturbance in the process of gametogenesis usually
involving a more or less complete lack of chromosome pairing at meiosis”.
King (1993) reports that a total of 22 reciprocal translocations and one X-autosome
translocation are known in the domestic pig (Sus scrofa), most of which have been detected
through the analysis of lineages exhibiting a decrease in litter size. The fertility effects vary from
a 25% reduction to total sterility.
King (1993) also reported that the structural heterozygote male offspring of Domestic sheep
carrying Robertsonian fusions presented aneuploidy in the gametes due to non-disjunction
during meiosis. It is interesting to notice how the frequency at which this occurred varied
between 6.9% and 20.2% (thus lower than expected) and that no aneuploid embryos were
recovered.
Baverstock et al. (1983) reported how F1 hybrids of Rattus colletti X Rattus villosissimus
survived but had reduced viability and fertility. Exams of male meiosis showed how three
trivalents and a chain of five were created (due to chromosomal differences) and the result was
a 70% litter reduction in backcrosses of the F1 to the parental forms. R.sordidus X R. colletti F1
crosses were completely sterile due to the presence of four trivalents, a ring of four and a chain
of seven in meiotic metaphase. In the same way, R. sordidus x R. villosissimus F1 crosses were
also totally infertile, as were the backcrosses (King 1993).
Hybridization studies between the tiny muntjac deer species (subfamily Muntiacinae) were
conducted by Liming et al. (1980) and Liming and Pathak (1981) and showed how F1 hybrids
between Muntiacus muntjac vaginalis X Muntiacus reveesi could be produced (both male and
female) but the hybrid male was completely sterile, as a result of spermatogenesis being
arrested at early prophase and degeneration of spermatocytes. King (1993) hypothesized that
the profound chromosomal differences between the morphologically similar Indian (Muntiacus
muntjac vaginalis ) and Chinese muntjacs (Muntiacus reveesi) were providing an absolute
reproductive barrier.

Page 32 of 177
The seven existing species of the Equidae family are characterized by extensive chromosome
differences with chromosome numbers varying from 2n=32 for Equus zebra hartmannae
(Hartmann’s zebra) to 2n=66 for E. przewalskii (Przewalski horse). F1 hybrids can be produced
between all species (King 1993), all but two of which are totally sterile, following a breakdown of
gametogenesis and general failure of meiosis at pachytene. The only two exceptions are the
hybrids between E. caballus (Common horse) and E. przewalskii (Przewalski horse) which are
differentiated by a single chromosome fusion (Short et al. 1974) and where, during the course of
meiosis, the heterozygous chromosomes form trivalents and segregate normally. F1 hybrids
and backcrosses to E. przewalskii are totally fertile. It is interesting to note that E. caballus is
thought to be directly descended, via a single speciation event, from E. przewalskii.
The other exception within the Equidae family is more interesting, since it has been considered
non-viable for a very long period of time. Interspecific hybrids between E. asinus and E.
caballus (male donkey X female horse) produce male and female mules, while male and female
hinny are produced by the reciprocal cross (male horse x female donkey). The traditional
viewpoint on both these F1 crosses was that they were sterile due to karyotypic incompatibility.
This view was somewhat modified by Zong and Fan (1989) who demonstrated how occasional
Mule and Hinny F1 hybrids could in fact be fertile and could be backcrossed to either of the
parental forms. Zong and Fan showed how all 8 backcross progeny that they analyzed carried
unique chromosome complements with a variability between 2n=60 to 2n=64 and very different
proportions of acrocentric and metacentric chromosomes. Only one of the hybrids analyzed
presented a horse-like karyotype.
The five species of African dik-diks and their threatened status have been the center of a wide
effort focused on breeding them in zoos that has brought to light an intricate system of
chromosomal variation within the species complex. In three specimens of Madaqua guentheri
examined in captivity (Ryder et al. 1989) two different karyotypes (2n=48 and 2n=50) were
identified which were distinguished by a chromosomal fusion/fission difference. Hybrids of these
two forms reproduce in captivity. In stark contrast with this finding, specimens of Madaqua kirki
were found by Ryder et al. to present two distinct cytotypes characterized by multiple
rearrangements, including an X-autosome translocation, inversions and tandem fusions which
resulted in only females of the hybrid being capable of generating progeny and male hybrids
being sterile due to spermatogenesis being arrested (despite extensive meiotic activity).
Hybridization between female M. kirki and male M. guentheri produced both male and female
F1 hybrids both of which were completely sterile. The results were interpreted by Ryder as
showing how the multiple distinguishing cytotypes of M.kirki were responsible for the
reproductive isolation between species and cytotypes. King (1993) commented that “Indeed, in
the examples provided, the more profound the chromosomal differences were between species,
or cytotypes, the greater was the degree of hybrid inviability or sterility”.
Analysis of the genus Lemur has shown a complex pattern of chromosomal reorganization
characterized by multiple rearrangements, the majority of which appear to be Robertsonian
fusions (Rumpler and Dutrillaux, 1976). Ratomponirina et al. (1988) analyzed the different
chromosomal complements and identified a total of 32 rearrangements, 29 of which are fusions,
spread among six species and seven subspecies. Crosses between five of the species of the
complex showed an increasing pattern of sterility directly correlated with the degree and
complexity of number of trivalents, or multivalents, created at meiosis, with results ranging from
minor effects on fertility to almost complete sterility. These results were interpreted by
Ratomponirina et al (1988) and Dutrillaux and Rumpler (1977) as being indicative that
Robertsonian rearrangements that form multiples at meiosis are a powerful reproductive barrier
and associated with speciation in lemurs.

Page 33 of 177
The marsupial Rock wallabies of the genus Petrogale were analyzed by Sharman et al (1990)
and 20 different karyotypes were identified, 11 of which are recognized as species.
Chromosomal fusion and fissions were the prevalent differences and, where parapatric in the
wild, hybrid zones were observed. Hybrids between chromosomal races differing by fusions
produced totally sterile males (where quadrivalents or pentavalents were formed at meiosis)
with females also presenting severely reduced fertility. Even males produced by a cross with
lesser degree of chromosomal differences (trivalent formed at meiosis) showed complete
sterility due to the production of abnormal spermatids.
The Australian grasshopper Caledia captiva is characterized by multiple cytotypes, two of which
are recognized as subspecies (Shaw et al. 1986) and show reduced fertility rates that can be
both derived from chromosomal effects (42% of the cases) or genetic divergence (58%). This
calculation was made possible by the fact that, amongst the cytotypes, there are crosses with
maximum chromosomal divergence and minimal genetic divergence as well as the reciprocal,
and a comparison could be made for the effects of both types of divergence.
In Mus domesticus (common mouse) King (1993) reports how heterozygotes for single fusions
showed a 2-28% reduction in fertility for males and a 33-61% reduction in females. These
effects increased in correlation with the amount of independent fusions present (albeit not in a
simply additive fashion). If chain multiples were formed at meiosis, males were completely
sterile or inviable but females were not (significant reductions of oocytes were observed). When
reciprocal translocations between autosomes and sex chromosomes were present, unpaired
elements or trisomics arose which caused male sterility and impaired female fertility.
In the Helianthus sunflower species complex, Riesenberg (1995a,b,1999,2000,2001) reports
how multiple chromosomal rearrangements have significant effects on hybrid fertility. Crosses
between H. annuus and H. petiolaris are self-incompatible annuals, with haploid chromosome
numbers of 17. They show seven collinear chromosomes between the two species, whereas
the remaining 10 chromosomes differ structurally due to a minimum of seven interchromosomal
translocations and three inversions. These structural changes generate multivalent formations
and bridges and fragments in hybrids leading to semi-sterility. F1 pollen viabilities are typically
less than 10% and seed set is less than 1%. Riesenberg proceeds then to point out to the role
of chromosomal rearrangements in speciation in Helianthus and how the chromosomal
differences can play a role in preventing introgression from the species of origin.
1.3. METHODS FOR PREDICTING FIXATION OF CHROMOSOMAL TRANSLOCATIONS
The traditional way of examining the ratios of alleles within a freely interbreeding population is by
applying the Hardy-Weinberg equilibrium to the allele frequencies that need to be modeled in order to
obtain the equilibrium frequencies that occur.
The Hardy–Weinberg equilibrium states that allele and genotype frequencies in a population will remain
constant from generation to generation in the absence of other evolutionary influences. These
influences include mate choice, mutation, selection, genetic drift, gene flow and meiotic drive.
Because one or more of these influences are typically present in real populations, the Hardy–Weinberg
principle describes an ideal condition against which the effects of these influences can be analyzed.
In the simplest case of a single locus with two alleles denoted A and a with frequencies f(A) = p and f(a)
= q, respectively, the expected genotype frequencies are:
f(AA)=p2 for the AA homozygotes
f(aa)=q2 for the aa homozygotes
f(Aa)=2pq for the Aa and aA heterozygotes

Page 34 of 177
The genotype proportions p2, 2pq, and q2 are called the Hardy–Weinberg proportions. Note that the
sum of all genotype frequencies of this case is the binomial expansion of the square of the sum of p
and q, and such a sum, as it represents the total of all possibilities, must be equal to 1. Therefore (p +
q)2 = p2 + 2pq + q2 = 1. A solution of this equation is q = 1 − p.
If union of gametes to produce the next generation is random, it can be shown that the new frequency f'
satisfies f'(A)=f(A) and f'(a)= f(a). That is, allele frequencies are constant between generations.
The values for each allele therefore depend exclusively on the starting values and rapidly converge to
fixed values as can be seen in figure 1.3 below.
Figure 1.3.: Hardy–Weinberg proportions for two alleles: the horizontal axis shows the two allele
frequencies p and q and the vertical axis shows the expected genotype frequencies. Each line shows
one of the three possible genotypes.
Given that the case at hand, nominally negatively heterotic chromosomal translocations, is
characterized by gametes of translocated individuals showing reduced fertility when crossed with non-
rearranged individuals we cannot utilize the Hardy Weinberg equilibrium directly as it is. It is, in fact,
necessary to account for the differential fitnesses of the possible crosses, thus affecting the selection
portion of the evolutionary influences that can affect Hardy Weinberg frequencies.
In a similar way we can also address the possibility of non-random mating, specifically the appearance
of so-called reinforcement genes which prevent its bearers from mating with specific types of
individuals.
By appropriate modifications of the Hardy Weinberg equilibrium, as shown in the materials and
methods section, we can model the effects of hybridization and influx of Wild Type individuals into the
new population as well as the results of the arising of Reinforcement genes.
The results will be presented and discussed in the discussion section.
1.3.1. The role of population size
The fact that large populations make the fixation of negatively heterotic chromosomal changes
extremely unlikely is a well-documented fact in literature. Riesenberg (2001) states that “the primary

Page 35 of 177
difficulty with most chromosomal models is that the fixation of strong underdominant chromosomal
rearrangements through drift is unlikely, except in small inbred populations” and his view is confirmed
by multiple other authorities such as Walsh (1982), Lande (1985), Turelli (2001) and Hedrick (1981).
King (1993) summarized the role of population size as follows:
“Empirically, it would seem unlikely that a chromosomal variant which is negatively heterotic would
have much chance of fixation in a population because of the reduced fertility it carries. Nevertheless,
such rearrangements do reach fixation and it is simply a matter of expanding our concept of population
genetics to account for these phenomena.”
Lande (1979) argued that stochastic processes and genetic drift would be sufficient to justify fixation of
negatively heterotic chromosomal rearrangements in populations of 100 interbreeding individuals or
less, especially when within the framework of strongly subdivided populations and high rates of local
extinction and re-colonization, which he argued were typical characteristics of many modern-day
species.
White (1978) argued that the most important factors in fixation of negatively heterotic rearrangements
were Genetic drift, meiotic drive and inbreeding.
Lande (1979) stated that “Local fixation or establishment of an underdominant mutation (with a
substantial heterozygote disadvantage), such as a major chromosomal rearrangement, has an
appreciable chance of occurring by random genetic drift only in a strongly subdivided population with
small, nearly isolated demes”.
Chesser and Baker (1986) published a computer simulation to determine the stochastic factors that
were required for fixation of chromosomal mutations in small isolated demes. This model included
several additional parameters not previously examined such as litter size, age-dependent mortality,
overlapping generations and varying sex ratios. Strangely enough, they didn’t account for inbreeding
between close relatives. They analyzed different impacts on the fertility of the heterozygotes (between
0 and 0.5).
The results of Chesser and Baker (1986) were that random processes alone were sufficient to
explain the frequency of fixation of chromosomal rearrangements when the number of initial
founders was small (5 to 10 individuals), the meiotic fertility effect limited and there was a high number
of offspring per mating. When population bottlenecks were larger than 20 individuals, random
processes could no longer explain fixation for rearrangements with substantial fertility effects. The
population cutoff number for fixation of rearrangements with a low impact on fertility was seen to be
between 20 and 50 individuals.
Walsh (1982) analyzed the rate at which reproductive isolation occurred and pointed out that
chromosomal speciation can only result from mildly to strongly heterotic rearrangements inducing
hybrid sterility if the populations were very small (less than 50 individuals) with a high chance of
extinction and inbreeding depression.
Based on the available literature and the population genetics models, it is safe to state that, within large
interbreeding populations, Chromosomal rearrangements are lost from the gene pool in one or very few
generations.
On the contrary, very small populations (ideally less than 20 individuals) and inbreeding can result in
fixation of Chromosomal rearrangements in local groups via stochastic factors.

Chromosomal rearrangements as speciation mechanisms - CRC Thesis

Chromosomal rearrangements as speciation mechanisms - CRC Thesis

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