1. Spiggs in Space: evolution and biogeography of stickleback armor
across Vancouver Island, BC, Canada watersheds.
Anela Layugan ‘17, Zoe LaFrance-Armstrong ‘16, Meyru Bhanti ‘17, Jingzhu Hao ‘17, Kristen Sheldon ‘17, Meredith Houghton ‘17, Sam Most ‘17, Carly Johnson ‘17, Natalya Specian ’17
Sponsors: Rich King & John Baker, Department of Biology
Acknowledgments:
This
work
was
supported
in
part
by
a
Na4onal
Geographic
grant
to
Dr.
Susan
Foster.
We
also
wish
to
thank
the
BC
field
crew.
Background
Our Approach
Adaptive radiations can offer unique insights into evolutionary processes,
enhancing our understanding of the ways in which diversification is initiated at the
onset of environmental change, as well as elucidating the processes by which the
evolution of new species occurs (King et al., 2016). One of the most promising
sources of insight is found in the post-glacial freshwater adaptive radiation of the
threespine stickleback fish, Gasterosteus aculeatus. However, many populations
are at risk of extinction through human-caused environmental change & species
introductions. Loss of novel diversity in sticklebacks limits, for example, our
understanding of the evolution & expression of genes important in skeletal
development in other vertebrates, including humans.
Ectodysplasin (Eda) and Paired-Like Homeodomain 1 (PitX1) are highly conserved
in vertebrates and are the major controlling loci for lateral plates and the pelvic
girdle in sticklebacks, respectively. These structures function together to form a box
around the fish, thus aiding in predator escape if captured (Reimchen, 1994).
Ancestral populations are generally fixed for complete lateral plate morphs and full
pelvic girdle expression (e.g., Bell & Foster, 1994) due to the large number of
piscivorous predators and high ion concentration in the ocean.
However, post-glacial, derived populations could experience both relaxed selection
from predators and selection against full expression of armor traits in the relatively
low-ion regime of freshwater lakes (Barrett et al., 2010). Additionally, a small
number of populations are polymorphic for plate (complete, partial, low; sensu Bell,
1976) and/or pelvic girdle expression either via fluctuating selection (Reimchen,
2000) or gene flow from nearby oceanic (i.e., anadromous) populations.
The natural hydrological regime and stream connectivity in many watersheds is
altered for anthropocentric benefit, often inhibiting movement of fish up or
downstream. Even though the design of modern dams and weirs considers
biological impacts, movement of small fish such as stickleback is restricted with
even the smallest of impediments (Raeymaekers et al., 2008). Moreover, many
lakes are stocked with non-native piscivorous species such as Rainbow & Cutthroat
Trout, changing the selection regime and thus leading to the loss of some low-
armor, stickleback populations (Baker et al., 2010).
Here we take advantage of the stickleback freshwater radiation & our
understanding of the ecological & genetic factors in body armor trait expression to
explore how gene flow, natural selection, & population loss shapes the geographic
distribution of body armor morphs in four watersheds on Vancouver Island, BC.
Discussion
Biogeography
Evolution
Learn More!
Data Acquisition
Principal Components Analysis
Correlation of ‘Armor Scores’
with lake chemistry & predators
Multiple Regression
Watershed Mapping
Population Collections
Nimpkish
River
Cowichan
River
Comox
Valley
Campbell
River
+/+
+/-­‐
-­‐/-­‐
Gene
Flow
Dis4nct,
but
very
closely-­‐linked
loci
regulate
different
aspects
of
bony
armor
plates
in
s4cklebacks.
Armor
plate
height
and
width
were
separately
fine-­‐mapped
using
thousands
of
F2
fish
from
a
gene4c
cross
between
a
large-­‐plated
marine
s4ckleback
and
an
armor-­‐reduced
freshwater
s4ckleback.
The
two
QTL
intervals
(red
and
green
bars)
barely
overlap.
(from
Indjeian
et
al.,
2016)
Body
shape
is
a
set
of
correlated
gene4c
and
environmentally
plas4c
traits.
Lake
depth,
habitat
complexity
(i.e.,
vegeta4on),
food
sources
(i.e.,
plankton
vs
benthos),
and
salinity
have
been
linked
to
overall
body
shape
changes
resul4ng
in
the
limne4c-­‐benthic
con4nuum
ubiquitous
in
s4ckleback
shape
studies
(e.g.,
Bell
&
Foster,
1994).
Our
data
suggests
that
maximum
body
depth
and
ventral
body
width
may
also
be
linked
to
selecDon
on
skeletal
armor
features.
Lateral
plate
phenotype
is
largely
controlled
by
EDAC
and
EDAL
alleles
with
a
number
of
puta4ve
and
unknown
enhancer
loci
(
e.g.,
see
ChrXX
to
the
leY).
Here
we
assume
par4al
dominance
of
the
EDAC
allele
for
lateral
plate
morph
(i.e.,
complete,
par4al,
low)
expression.
Contrary to expectations, neither predator regime, lake size, nor tannins
explained variation in armor traits in our data. Reimchen (2013) found in nearby
Haida Gwaii populations that fish predators tended to account for more robust
armor phenotypes, but that this was modified by an interaction between lake
size and water color (i.e., tannins). This same study did not find a correlation
between armor and ions while Bell (2000) and Smith et al., (2014) both found
significant correlations, though in opposite directions.
We found that armor was negatively correlated with ion concentration in
freshwater populations, a counterintuitive outcome. Ions in general, and Ca++
availability specifically should allow for greater boney armor development.
However, predators could drive armor defense traits primarily, and if ions are
limited then a trade-off with other traits would be expected. In low pH lakes
(such as most within our study area) Ca++ is limited and armor incurs a greater
energetic investment as ions decrease in availability. This may play out as a
cost to growth and/or reproduction that we did not consider in the current study.
Nevertheless, it remains unclear why a negative correlation between armor and
ions exists in our study or in Bell’s (2000) study of Alaskan populations.
Perhaps the most interesting pattern we’ve uncovered is seen simply in the
biogeographic distribution of plate morphs and in the variation across
watersheds and putative ancestral (oceanic) stocks. Plate polymorphisms exist
in oceanic populations around Vancouver Island, but appear to be restricted to
lower salinity Georgia Strait and Strait of Juan de Fuca populations (see map
immediately below). The possibility of significant genetic variation in founding
stocks at the watershed scale is intriguing and has not been widely considered.
Freshwater populations are adapted to local conditions as is commonly
described for post-glacial stickleback (e.g., Bell & Foster, 1994). Although,
watershed-level phenomena can limit adaptation, a fact not typically considered
in most studies. In our watersheds, gene flow is widely variant with, for example,
Nimpkish watershed exhibiting upstream gene flow but not downstream, and
Campbell watershed showing only downstream gene flow due to a dam
precluding upstream movement. In Nimpkish lakes, high levels gene flow
maintains a plate polymorphism even though local selection likely acts against
high plate morphs. In Campbell River lakes, upstream migration is halted by the
John Hart Lake Dam, thus upstream populations have become fixed for low
plate morph, but in this watershed introduced predators, cutthroat and rainbow
trout, may have played a role in the loss of some low-armor populations.
Projected
Coordinate
System:
NAD83
Environment
BC
Albers.
Data
Sources:
Bri4sh
Columbia
Ministry
of
Energy,
Mines
and
Petroleum
Resources;
Bri4sh
Columbia
Ministry
of
Environment;
GeoGra4s.
Contains
informa4on
licensed
under
the
Open
Government
License
–
Canada.
Maps
created
by
A.
Layugan.
Scale
bars
for
each
watershed
~25km.
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Three-­‐dimensional
plots
showing
PC1-­‐PC1,
Armor
Box,
Body
Shape,
and
Lateral
Plates
respec4vely
by
watershed.
Red
are
for
the
oceanic
popula4ons
and
blue
is
the
freshwater
popula4ons.
All
axes
are
ploged
on
the
same
scale
but
separately
by
watershed
for
clarity.
Note
that
the
oceanic
types
reside
in
different
3D
‘Armor
Space’,
an
important
point
for
inferring
direc4on
of
evolu4onary
change
in
this
system.
Nimpkish
River
Cowichan
River
Comox
Valley
Campbell
River