4. Food, shelter, water
# of animals, protection, hiding spots
Conspecifics, mate choice, pair bond
Mating behaviors, parenting
experience
Success
Breeding Needs
5. Food, shelter, water
# of animals, protection, hiding spots
Conspecifics, mate choice, pair bond
Mating behaviors, parenting
experience
SuccessSperm competition
Cryptic female choice Individual oddities
Genetics (MHC)
6. Specific Causes of Infertility
• Recessive genes
• Gamete incompatibility
• Polyspermia fertilization
• Production errors
• Lack of fertilization
• Poor parental care
8. New Theories & Associations
• Major Histocompatibility Complex (MHC) gene
• Pathogen driven selection
• Heterozygotes preference
• Sexual selection
• Reproductive selection
9. New Theories & Associations
• Major Histocompatibility Complex (MHC) gene
• Pathogen driven selection
• Heterozygotes preference
• Sexual selection
• Good/complementary genes
• Reproductive selection
AA
A
B
BBBB
A
B
AA
AA
AB
BBBB
AB
AA
10. New Theories & Associations
• Major Histocompatibility Complex (MHC) gene
• Pathogen driven selection
• Heterozygotes preference
• Sexual selection
• Good/complementary genes
• Reproductive selection
11. New Theories & Associations
• Major Histocompatibility Complex (MHC) gene
• Pathogen driven selection
• Heterozygotes preference
• Sexual selection
• Good/complementary genes
• Reproductive selection
• Avoiding in breeding
12. MHC and Infertility
• Multifactorial and poorly understood
• Artificial Insemination
• Effects of MHC similarity lost following AI!
• Let’s look at some data!
16. Future Breeding Avenues
What We Know
• Some birds are able to
select mates based off of
MHC gene; others don’t
have a bias
• Birds utilize post-copulatory
mechanisms that may
contribute to infertility rates
• Infertility can be difficult to
assess in birds as there are
multiple factors to consider
at many levels
What We Don’t Know
• Is infertility directly
associated with the MHC
gene?
• We can look back into our
infertile breeding pairs to
see if they had MHC similar
genes
• Can we use the MHC
gene to pre-screen pairs in
order to increase breeding
success and fertility rates?
17. Summary
• Hierarchy of needs for breeding success
• Causes & strategies of infertility
• New theories and associations
• Future breeding avenues
19. References
Baratti, M., F. Dessi-Fulgheri, R. Ambrosini, A. Bonisoli-Alquati, M. Caprioli, E. Goti, A.
Matteo, R. Monnanni, L. Ragionieri, E. Ristori, M. Romano, D. Rubolini, A. Scialpi, N. Saino.
2012. MHC genotype predicts mate choice in the ring-necked pheasant Phasianus colchicus.
Journal of Evolutionary Biology 25: 1531-1542.
Bonneaud, C., O. Chastel, P. Federici, H. Westerdahl, and G. Sorci. 2006 Complex MHC-
based mate choice in a wild passerine. Proceedings of the Royal Society 273: 1111-1116
Collet, J., D.S. Richardson, K. Worley, T. Pizzari 2012. Sexual selection and the different
effects of polyandry. Proceedings of the National Academy of Sciences 190 (22): 8641-8645
Dean, R., CK Cornwallis, H Lovile, K Worley, D Richardson, and T Pizzari. 2010. Male
reproductive senescence causes potential for sexual conflict over mating. Current Biology 20:
1192-1196.
Dean, R., S. Nakagawa, T. Pizzari. 2011. The Risk and Intensity of Sperm Ejection in
Females Birds. The American Naturalist 178 (3): 343-354.
Ginzburg, A.S. 1972. Fertilization in Fishes and the Problem of Polyspermy. Israel Program
for Scientific Translations, Jerusalem
20. References Continued
Hemmings, N., M. West, T.R. Birkhead. 2012. Causes of hatching failure in endangered
birds. Proceedings from the Royal Society Dec 23 (6): 964-967
International Crane Foundation. Flock egg data. 2014.
Jones, R.C. and M. Lin. 1993. Spermatogenesis in Birds. Oxford Review Reproductive
Biology 15:233-264
Loisel, D.A., S.C. Alberts, and C. Ober. 2007. Functional significance of MHC variation
in mate choice, reproductive outcome, and disease risk. Duke University 95-108.
Morrow, E.H, G. Arnqvist, & T.E. Pitcher. 2002. The evolution of infertility: does hatching
rate in birds coevolve with female polyandry? Journal of Evolutionary Biology. 15: 702-
709.
Nicolich, J.M., G.F. Gee, D.H. Ellis, S.G. Hereford. 2001. Natural Fertility in Whooping
Cranes and Mississippi Sandhill Cranes at Patuxent Wildlife Research Center. North
American Crane Workshop Proceedings 8:170-177.
21. References Continued
Pizzari, T., H. Lovlie, and CK Cornwallis. 2004. Sex-specific, conuteracting
responses to inbreeding in a bird. Proceedings of the Royal Society 271: 2115-2121
Pizzari, T., DP Froman, and TR Birkhead. 2002. Pre- and post-insemination episodes
of sexual selection in the fowl, Gallus g. domesticus. Heredity 88:112-116.
Pizzari, T. C.K. Cornwallis, and D.P. Froman. 2007. Social competitiveness
associated with rapid fluctuations in sperm quality in male fowl. Proceedings of the
Royal Society 274: 853-860.
Pizzari, Tommaso. 2009. Sexual Selection: Sperm in the Fast Lane. Current Biology
19 (7): R292-R294.
Richardson, DS, J. Komdeur, T. Burke, T. von Schantz. 2005. MHC-based patterns
of social and extra-pair mate choice in the Seychelles warbler. Proceedings of the
Royal Society 272: 759-767
22. References Continued
Rymesova, Dana. 2013. Survival and mate choice in the grey partridge Perdix
perdix. Masaryk University Faculty of Science Department of Botany and Zoology,
PhD dissertation.
Strandh, M., H. Westerdahl, M. Pontarp, B. Canback, MP Dubois, C. Miquel, P.
Taberlet, and F. Bonadonna. 2012. Major histocompatibility complex class II
compatibility, but not class I, predicts mate choice in a bird with highly developed
olfaction. Proceedings of the Royal Society 27: 4457-4463
Zheng, W.M., M. Nishibori, N. Isobe, and Y. Yoshimura. 2001. An in situ
hybridization study of the effects of artificial insemination on the localization of cells
expressing MHC class II mRNA in the chicken oviduct. Reproduction 122: 581-586
Editor's Notes
Looking at the hierarchy of needs for breeding success in birds
Discuss causes and strategies of infertility
Present some new theories and associations for mate choice in relation to breeding success and the MHC gene
And finally, I’ll wrap up with some data from the ICF and present some ideas to overcome infertility rates for future breeding
Maslow’s hierarchy of needs.
Adapt it to the breeding needs of birds in order to have reproductive success.
For those who are unfamiliar with Maslow’s hierarchy of needs, it’s a theory of human motivation in which to advance to the next level of the pyramid, you need to acquired the components of the previous step.
We’ll start here {ANIMATION} with the basics and continue to work our way up. Along the way I’ll state ways in which management and animal care can contribute to a bird’s reproductive success.
We start at the bottom with
Physiological needs such as food, shelter, water. Pretty self explanatory here, but these first two steps are where we, management/animal care takers, can have the most influence on and most important as we want to set our birds up for reproductive success.
-We want to provide a diet that is completely nutritious or ideally best mimics their diet in the wild.
- We want to provide enclosures that are large enough to allow the bird to exhibit their natural behaviors including breeding and hiding.
- basically a happy and healthy bird is what we’re trying to achieve at this step.
{ANIMATION}
The next step is Safety & security. We know that some species of birds (flamingos) like safety in numbers where as others, such as breeding cranes, do best as individual breeding pairs and that are kept away from other breeding pairs. We can achieve success in this step through our enclosure design and keeping in mind things that will help a bird feel more safe and secure such as providing hiding spots and protection.
- Protection includes using materials that are strong enough to withhold the elements and external forces, such as predators or falling limbs, while at the same time, keeping the animals in and minimizing individual injury.
- Hiding spots are necessary and allows them to display natural behaviors from predators which can include other animals and humans or their conspecifics.
( It’s recommended to have an empty enclosure between breeding pairs of cranes, creation of a visual barrier, or alternatively, providing a 1-2 m gap between adjacent enclosures to avoid aggression through the fence. )
{ANIMATION}
Love & belonging: I’m going to say that this stage is where birds need to know their conspecifics, choose a mate, form that essential pair bond in monogamous species such as cranes. From a management stand point, we influence this step through SSP breeding recommendations, our exhibit design, and intervening when needed if birds become too aggressive with each other. This step can also include puppet rearing chicks and introducing them to large social groups at the appropriate time to learn what they need to accomplish in order to be successful in the next step.
{ANIMATION}
The next step is Experience. With time, hopefully, birds will gain confidence in what courtship displays, vocalizations, doing the deed, and parenting skills is all about. For those that never ‘get it’, management can step it with tools such as artificial incubation, hand/puppet rearing, or artificial insemination to help achieve success.
{ANIMATION}
Finally, if all previous steps are achieved, we’ve reached (in theory) success in breeding!
But as with all things in life, it’s never that simple. {ANIMATION}
There are other biological factors and components that play a role in the success and fertility rates in birds. Some are well understood and some are not. Some causes of infertility we’ll discuss today include: pre and post-copulation strategies such as {ANIMATION} cryptic female choice, {ANIMATION}sperm competition, {ANIMATION} genetics, and {ANIMATION} individual oddities.
Let’s dive into this…
Specific causes that contribute to infertility rates include1:
Recessive genes or lethal alleles (an example of this is a homozygous Manx cat)
Gamete incompatibility (segregation disorters, cytoplasmic parasites, maternal lethal effects)
Polyspermia fertilization (>1 sperm fertilizes egg causing embryo death from inappropriate number of chromosomes)
Production errors (such as a female producing a bad egg or entering reproductive senescence)
Lack of fertilization (this has both female and male components…we’ll focus more on this next)
And finally, poor parental care (not incubating appropriately, poor nest choice, poor parental care post-hatching)
All of these causes can {ANIMATION} lead to death and thus contribute to infertility rates
Reference:
1 Morrow, E.H, G. Arnqvist, & T.E. Pitcher. The evolution of infertility: does hatching rate in birds coevolve with female polyandry? Journal of Evolutionary Biology. 15: 702-709. 2002
Females are able to utilize a couple of post-copulation strategies that may influence infertility rates. The first is sperm ejection {ANIMATION}. Sperm ejection is just as it sounds. Females are able to eject the sperm that has just been inseminated in them. In the domestic chickens, on average 80% of a male’s ejaculate can be ejected1. It is thought that this strategy was evolved as a more subtle way to reject males than to fight them off1.
The second strategy females use is cryptic female choice {ANIMATION}. This is the ability of a female bird to preferentially choose a specific male’s sperm to fertilize her egg2. They can stores viable sperm for approximately 2 weeks in their sperm storage tubules3. Females can select sperm in favor of a specific phenotype2 or other characteristics such as MHC compatibility.
For males, {ANIMATION} poor sperm quality (morphology and motility) and quantity can contribute to infertility rates. Older males tend to have poorer sperm9 which decreases their overall chance for survival and to fertilize an egg. A study in domestic chickens noted that sperm quality varied (most likely due to seminal fluid composition rather than spermatogenesis itself) following a social challenge. Dominate males had sperm mobility that peaked before the challenge and then dropped 2 weeks after the challenge, whereas non-dominate males had sperm that were constant in mobility throughout the challenge and then slightly increased after the challenge4. In this case, if a non-dominate male’s sperm was able to out-complete and fertilize the ova when the dominate male’s sperm is less mobile, the poorer sperm could still contribute to post-fertilization infertility rates because it’s a poor doer.
{ANIMATION}
From an evolutionary stand point, sperm competition has resulted in overly efficient sperm5. Sperm are able to swim faster and live longer6. By swimming faster, they get to storage tubules first and can remain competitive over time, therefore increasing their chances of fertilizing an ova2, 6. Spermatogenesis in birds is 4xs faster than mammals and birds can produce 4xs as much sperm compared to mammals7. (Their sperm cycle takes only 3 days7.) It’s thought that the high sperm production is associated with the need to breed multiple females over days-weeks7 to increase the chances of reproductive success.
With more competitive sperm, females have also evolved mechanisms to prevent Polyspermia. {ANIMATION} Females have made molecular and structural adaptations to their eggs which make it more difficult for sperm to fertilize5. Although the female’s adaptation may have evolved to prevent polyspermia and loss of an embryo, you can imagine that this strategy only propagates sperm competition. There have been reviews that showed polyspermy rates in natural populations of fish can be as high as 30-40% percent5,8. And I’m not sure of the rate in birds.
A big question that remains unanswered is how much of this battle of sperm competition and sturdier eggs to prevent polyspermia are actually related to infertility rates?
(Cortical reaction normally prevents >1 sperm fertilizing an egg.)
References:
1 Dean, R., S. Nakagawa, T. Pizzari. 2011. The Risk and Intensity of Sperm Ejection in Females Birds. The American Naturalist 178 (3): 343-354.
2 Pizzari, T., DP Froman, and TR Birkhead. 2002. Pre- and post-insemination episodes of sexual selection in the fowl, Gallus g. domesticus. Heredity 88:112-116.
3 Collet, J., D.S. Richardson, K. Worley, T. Pizzari 2012. Sexual selection and the different effects of polyandry. Proceedings of the National Academy of Sciences 190 (22): 8641-8645
4 Pizzari, T. C.K. Cornwallis, and D.P. Froman. 2007. Social competitiveness associated with rapid fluctuations in sperm quality in male fowl. Proceedings of the Royal Society 274: 853-860.
5 Morrow, E.H, G. Arnqvist, & T.E. Pitcher. The evolution of infertility: does hatching rate in birds coevolve with female polyandry? Journal of Evolutionary Biology. 15: 702-709. 2002
6 Pizzari, Tommaso. 2009. Sexual Selection: Sperm in the Fast Lane. Current Biology 19 (7): R292-R294.
7Jones, R.C. and M. Lin. 1993. Spermatogenesis in Birds. Oxford Review Reproductive Biology 15:233-264
8 Ginzburg, A.S. 1972. Fertilization in Fishes and the Problem of Polyspermy. Israel Program for Scientific Translations, Jerusalem
9 Dean, R., CK Cornwallis, H Lovile, K Worley, D Richardson, and T Pizzari. 2010. Male reproductive senescence causes potential for sexual conflict over mating. Current Biology 20: 1192-1196
Some new theories that have emerged is the association of the Major Histocompatibility Complex (MHC) gene with mate selection and its association with reproductive success.
The MHC gene plays a key role in our immune system. There are 3 classes that comprise the MHC gene and they constantly present antigens (both from self and foreign) to our immune system. These genes are quite diverse and over the past decade or so, have been investigated in respect to mate choice.
The three theories that are thought to tie mate choice with this gene are: {ANIMATION} pathogen driven selection, {ANIMATION} sexual selection, and {ANIMATION} reproductive selection.
{ANIMATION} Pathogen driven selection is a theory in which females would chose their mates based on their MHC genes such that a heterozygous chick will be more pathogen resistant than a homozygote and therefore will have an overall better fit for survival against pathogens. Species that have been studied based of this theory and support it include fish, sheep, snakes, and mice1. There was also a study on wild passerines that correlated mate choice based on MHC diversity for parasitic diversity to resistance.2
References: 1 Loisel, D.A., S.C. Alberts, and C. Ober. 2007. Functional significance of MHC variation in mate choice, reproductive outcome, and disease risk. 95-108.
2 Bonneaud, C., O. Chastel, P. Federici, H. Westerdahl, and G. Sorci. 2006 Complex MHC-based bate choice in a wild passerine. Proceedings of the Royal Society 273: 1111-1116
{ANIMATION} Sexual selection is a theory based on selecting a mate whose MHC characteristics will improve the overall fitness of offspring based on the genetics of having good genes vs complementary genes. For example, {ANIMATION} n this image, gene A is the “good genes” that will improve overall fitness of an offspring. All females in this scenario would want to mate with this male (AA) as mating with other males will decrease genetic fitness. On the other hand, {ANIMATION} females can select mates based on the “complementary genes” hypothesis because each scenario would result in a heterozygote offspring1.
References: 1 Loisel, D.A., S.C. Alberts, and C. Ober. 2007. Functional significance of MHC variation in mate choice, reproductive outcome, and disease risk. 95-108
***There have been studies in birds and other species that support both mate choice with MHC genes for both the good and comparable gene hypothesis. For example:
{ANIMATION} Ring Necked Pheasants- females avoided MHC identical males (good) 3
{ANIMATION} Blue Petrels- MHC predicted mate choice as females chose males who had different MHC to maximize genetic diversity (complementary) 4
{ANIMATION} Seychelles Warbler- showed no MHC preference, however if the primary mate had a low # of MHC alleles, she’d perform extra-pair mating with a male of greater genetic diversity (complementary) 5
{ANIMATION} Grey Partridge- # of MHC alleles was not associated with pairing success. However, MHC IIB can play a role in mate choice based on complementary hypothesis6
References:
3 Baratti, M., F. Dessi-Fulgheri, R. Ambrosini, A. Bonisoli-Alquati, M. Caprioli, E. Goti, A. Matteo, R. Monnanni, L. Ragionieri, E. Ristori, M. Romano, D. Rubolini, A. Scialpi, N. Saino. 2012. MHC genotype predicts mate choice in the ring-necked pheasant Phasianus colchicus. Journal of Evolutionary Biology 25: 1531-1542.
4 Strandh, M., H. Westerdahl, M. Pontarp, B. Canback, MP Dubois, C. Miquel, P. Taberlet, and F. Bonadonna. 2012. Major histocompatibility complex class II compatibility, but not class I, predicts mate choice in a bird with highly developed olfaction. Proceedings of the Royal Society 27: 4457-4463.
5 Richardson, DS, J. Komdeur, T. Burke, T. von Schantz. 2005. MHC-based patterns of social and extra-pair mate choice in the Seychelles warbler. Proceedings of the Royal Society 272: 759-767
6 Rymesova, Dana. 2013. Survival and mate choice in the grey partridge Perdix perdix. Masaryk University Faculty of Science Department of Botany and Zoology, PhD dissertation.
Reproductive selection is a theory based on {ANIMATION} avoiding in breeding. There was a study with blue petrels that associated odors to MHC genes and birds were able to recognize their family members and avoid breeding with them4. Earlier we discussed the utilization of cryptic female choice and sperm ejection. Both of these post-copulatory mechanisms can allow females to avoid in breeding as well. In one study of red jungle fowl, males tended to ejaculate more sperm into related females when unrelated females were not present for breeding7. The females were able to reduce the probability of inbreeding by utilizing the post-copulatory mechanisms. She tended to release more sperm form her storage tubules from unrelated males7. And in the domestic chicken, the MHC gene is expressed on the oviduct so she can be sperm selective8.
References:
4 Strandh, M., H. Westerdahl, M. Pontarp, B. Canback, MP Dubois, C. Miquel, P. Taberlet, and F. Bonadonna. 2012. Major histocompatibility complex class II compatibility, but not class I, predicts mate choice in a bird with highly developed olfaction. Proceedings of the Royal Society 27: 4457-4463.
7 Pizzari, T., H. Lovlie, and CK Cornwallis. 2004. Sex-specific, conuteracting responses to inbreeding in a bird. Proceedings of the Royal Society 271: 2115-2121
8 Zheng, W.M., M. Nishibori, N. Isobe, and Y. Yoshimura. 2001. An in situ hybridization study of the effects of artificial insemination on the localization of cells expressing MHC class II mRNA in the chicken oviduct. Reproduction 122: 581-586
With all the theories and hypothesis regarding the MHC gene and its relation to mate choice and breeding, I still haven’t directly answered whether or not there’s an association with this gene acting on infertility rates. Well, I hate to break it to you, but this gene is multifactorial and poorly understood. Research can be difficult to control the many factors that play a role in a bird’s reproductive success with 95% confidence. But what we can continue to explore what we can.
We do have evidence that performing artificial insemination in birds eliminates the effects of MHC genes on mate choice altogether. What this means for us is if we are presented with a pair of birds that are too genetically related and their fertility rate is low to non existent, we can try inseminating them and bypass the aspect of females choosing males with specific MHC gene.
This graph depicts the average fertility of all birds in the flock from 1991-2014 using artificial insemination. The overall average flock fertility is 45.8%3.
Infertility rates in natural populations can be very high1. There was a study that noted infertility rates can vary anywhere between 0-80%2.
There was a paper I came across assessing natural fertility in whooping cranes and mississippi sandhill cranes from 2001 at the Patuxent Wildlife Research Center. The average natural fertility rate of WC was 65% and MSC 66%4.
On average, 15% of eggs produced fail to hatch1.
References:
1 Morrow, E.H, G. Arnqvist, & T.E. Pitcher. 2002. The evolution of infertility: does hatching rate in birds coevolve with female polyandry? Journal of Evolutionary Biology. 15: 702-709
2 Hemmings, N., M. West, T.R. Birkhead. 2012. Causes of hatching failure in endangered birds. Proceedings from the Royal Society Dec 23 (6): 964-967
3 International Crane Foundation. Flock egg data. 2014.
4 Nicolich, J.M., G.F. Gee, D.H. Ellis, S.G. Hereford. 2001. Natural Fertility in Whooping Cranes and Mississippi Sandhill Cranes at Patuxent Wildlife Research Center. North American Crane Workshop Proceedings 8:170-177.
This graph depicts the fertility of intact eggs from the flock overall during the same time period. (It accounts for the # of eggs broken.) The average here was 54.34%.
So far it seems like there’s a roughly 50% chance a crane will lay a fertile egg and that egg will make it to its hatch date.
To dive a little deeper, I’ve graphed each individual dam’s overall fertility rate (blue), fertility of intact eggs (red), and overall hatchability rate (green) over the cross of her lifespan to date at their respective institutions. {ANIMATION} Here I’ve depicted the overall flock fertility rate of 45% in order to pick out the individual birds who management may want to investigate infertility issues.
These 3 birds here {ANIMATION} (red rhombus), have a 0% fertility rate. Looking back into the records, Angel is 9 years old and entered the breeding flock just 3 years ago. She has laid her first egg, but has not laid her first fertile egg. We can explain her infertility due to possible acclimation to a new environment and mate, or that she’s still young to lay fertile eggs. The data from ICF that was provided to me noted that these WC on average were 8 years old when they laid their first egg. It’s not until 3 years later, at 11 years of age, which they laid their first fertile egg.
Anzac is 11 years old and has laid eggs but all of her eggs have broken. {ANIMATION} Let’s assume that if our first 3 levels of our pyramid are stable, management can come in in this case to provide support by removing her eggs as soon as possible and artificially incubating them. Although in reality, her poor infertility assessment should start at the bottom of our pyramid.
Chip is 24 years old and has only laid 2 eggs and it is thought that her infertility issues may be due to a physiological reproductive issue.
Let’s turn our attention to {ANIMATION} Seurat who is 15 years old. She has a fertility rate of 4.7% but 100% success in hatching a chick. In her records, they note that she only lays eggs when she’s out on exhibit. Could this be an individual oddity with preferential selection for a specific environment? We don’t know.
Next, if we look at {ANIMATION} McGee she has been 100% fertile and has an overall hatchability rate of 80%. She has been the only bird that Is naturally serviced by a male. It would be great to assess her and her mate for their MHC gene variance, but unfortunately, she died last year.
My point is, although we can graphically depict an individual bird’s fertility rate and success over the years, there are many aspects that could explain their infertility and these could be occurring at any point on our pyramid of needs. It would be interesting to see if the MHC similarity of these birds with their mates and whether or not they would breed with each other naturally with the same rate of success as AI.
This brings us to some future avenues we can experiment with in relation to the MHC gene and decreasing infertility rates.
Let’s break it down to what we do know and what we don’t…
Drs. for assisting me with my project idea and pulling it all together
Everyone for making my short time with you a pleasant one filled with learning opportunities
