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Gill raker divergence is a general pattern in adaptive radiations of postglacial fish, but few studies have addressed the adaptive significance of this morphological trait in foraging and eco-evolutionary interactions among predator and prey. Here, a set of subarctic lakes along a diversifying gradient of coregonids was used as the natural setting to explore correlations between gill raker numbers and planktivory as well as the impact of coregonid radiation on zooplankton communities. Results from 19 populations covering most of the total gill raker number gradient of the genus Coregonus, confirm that the number of gill rakers has a central role in determining the foraging ability towards zooplankton prey. Both at the individual and population levels, gill raker number was correlated with pelagic niche use and the size of utilized zooplankton prey. Furthermore, the average body size and the abundance and diversity of the zooplankton community decreased with the increasing diversity of coregonids. We argue that zooplankton feeding leads to an eco-evolutionary feedback loop that may further shape the gill raker morphology since natural selection intensifies under resource competition for depleted prey communities. Eco-evolutionary interactions may thus have a central role creating and maintaining the divergence of coregonid morphs in postglacial lakes. KeywordsEcological speciation–Foraging trait–Polymorphism–Vendace–Whitefish morphs
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ORIGINAL PAPER
The role of gill raker number variability in adaptive
radiation of coregonid fish
Kimmo K. Kahilainen
Anna Siwertsson
Karl Ø. Gjelland
Rune Knudsen
Thomas Bøhn
Per-Arne Amundsen
Received: 24 February 2010 / Accepted: 13 July 2010 / Published online: 27 July 2010
Ó Springer Science+Business Media B.V. 2010
Abstract Gill raker divergence is a general pattern in adaptive radiations of postglacial
fish, but few studies have addressed the adaptive significance of this morphological trait in
foraging and eco-evolutionary interactions among predator and prey. Here, a set of sub-
arctic lakes along a diversifying gradient of coregonids was used as the natural setting to
explore correlations between gill raker numbers and planktivory as well as the impact of
coregonid radiation on zooplankton communities. Results from 19 populations covering
most of the total gill raker number gradient of the genus Coregonus, confirm that the
number of gill rakers has a central role in determining the foraging ability towards
zooplankton prey. Both at the individual and population levels, gill raker number was
correlated with pelagic niche use and the size of utilized zooplankton prey. Furthermore,
the average body size and the abundance and diversity of the zooplankton community
decreased with the increasing diversity of coregonids. We argue that zooplankton feeding
leads to an eco-evolutionary feedback loop that may further shape the gill raker mor-
phology since natural selection intensifies under resource competition for depleted prey
communities. Eco-evolutionary interactions may thus have a central role creating and
maintaining the divergence of coregonid morphs in postglacial lakes.
Keywords Ecological speciation Foraging trait Polymorphism Vendace
Whitefish morphs
K. K. Kahilainen
Department of Environmental Sciences, University of Helsinki, P.O. Box 65, 00014 Helsinki, Finland
K. K. Kahilainen (&)
Kilpisja
¨
rvi Biological Station, University of Helsinki, Ka
¨
sivarrentie 14622, 99490 Kilpisja
¨
rvi, Finland
e-mail: kimmo.kahilainen@helsinki.fi
A. Siwertsson K. Ø. Gjelland R. Knudsen T. Bøhn P.-A. Amundsen
Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and Economics,
University of Tromsø, 9037 Tromsø, Norway
T. Bøhn
GenØk Centre for Biosafety, The Science Park, P.O. Box 6418, 9294 Tromsø, Norway
123
Evol Ecol (2011) 25:573–588
DOI 10.1007/s10682-010-9411-4
Introduction
In adaptive radiation, a common ancestor is diverged into two or more species via eco-
logical processes and morphological adaptations to utilize different niches (Schluter 2000;
Grant and Grant 2008). Foraging trait evolution in relation to adaptive radiations has been
intensively studied in simplified and isolated ecosystems such as distant islands or their
continental counterparts, newly formed lakes (Dieckman et al. 2004; Losos and Ricklefs
2009). A classic text book example is the adaptive radiation of the beak size and shape
of Geospiza spp., where a common ancestor has diversified into a variety of species
specialized to feed on specific types of plant seeds within a wide range of seed sizes and
hardnesses (Grant and Grant 2008). In fishes, the adaptive radiation of East African
cichlids represents an excellent example of distinct morphological adaptations of head and
jaws correlated with specific foraging niches (Clabaut et al. 2007; Salzburger 2009).
However, adaptive radiations also occur in much less diverse environments such as in
many fish lineages in postglacial lakes (Schluter 1996). The general pattern is a divergence
along the pelagic-benthic resource axis, where morphological adaptations in body and head
shape seem to be important in the radiation process (Schluter and McPhail 1993; Robinson
and Parsons 2002; Amundsen et al. 2004a). We focus on one of these traits, the gill raker
number, as surprisingly few large scale studies have been made to reveal the adaptive
significance of this trait even though it is an important trophic trait in variety of fish species
(see e.g., Janssen 1980; Gibson 1988; Friedland et al. 2006).
Coregonid fishes have a circumpolar distribution with frequent co-occurrence of
multiple ecologically and morphologically distinct morphs (Sva
¨
rdson 1979; Bernatchez
et al. 1999; Amundsen et al. 2004b). Both ecological and genetic evidence suggests that
adaptive radiation is the most likely explanation for the observed patterns (Bernatchez 2004;
Østbye et al. 2006; Hudson et al. 2007). Different morphs of coregonids have traditionally
been identified from the number of gill rakers (Sva
¨
rdson 1952; Lindsey 1981; Bernatchez
2004) which is a heritable and ecologically important trait (Sva
¨
rdson 1979; Rogers and
Bernatchez 2007). The European whitefish (Coregonus lavaretus (L.)) is the most diverse
coregonid species, and has repeatedly and independently radiated from a common ancestor
into multiple morphs in a large number of postglacial lakes (Østbye et al. 2005). Genetic
results indicated similar divergence of pelagic and littoral morphs in replicate lakes sug-
gesting parallel evolution within each lake (Østbye et al. 2006). This previous study using
microsatellite data indicated that sympatric pelagic and littoral whitefish morphs are
genetically different (Østbye et al. 2006) and the vicinity of current study area with similar
morphs suggests that genetic differences are likely to exist. Due to highly similar radiation
patterns of morphs in different lakes, we clustered whitefish as three different groups
according to their specific ecomorphology. Here, whitefish exhibit distinct morphs for all
three principal lake habitats (i.e., the littoral, profundal and pelagic), in which each has
specific prey resources (Kahilainen et al. 2003, 2005; Jensen et al. 2008). The littoral is
structurally complex with diverse benthic resources, comprising a sharp contrast to the low
light conditions and scanty sediment-buried benthic resources in the profundal habitat (i.e.,
the deep benthic zone). The pelagic zone is a structurally homogenous habitat providing
zooplankton resources for fish. These principal lacustrine habitats can be considered as
peaks in an adaptive landscape that requires morphological adaptations to enhance utili-
zation of their specific diet resources. Accordingly, one should expect morphs from these
principal habitats to differ in important foraging related traits such as the gill raker
apparatus (Schluter and McPhail 1993; Robinson and Parsons
2002; Amundsen et al.
2004a).
574 Evol Ecol (2011) 25:573–588
123
The role of the gill raker apparatus is related to prey retention efficiency, where the gill
rakers function as a cross-flow filter (Sanderson et al. 2001; Smith and Sanderson 2008).
An increasing number of gill rakers enhance crossflow filtering and the closely spaced gill
rakers also limit the escape possibilities of small prey. However, a dense gillraker appa-
ratus is more likely to be clogged by sediments than more sparse gillrakers, and foraging in
the muddy bottom of the profundal most likely require other gillraker adaptations.
Accordingly, a high number of long gill rakers is common in planktivorous fish species and
morphs, whereas benthic species and morphs usually display a lower number of shorter gill
rakers (Janssen 1980; Schluter and McPhail 1992; Robinson and Parsons 2002). Corego-
nids have a wider gillraker range than other polymorphic fish lineages and thus represent
an excellent candidate taxon to evaluate the significance of such phenotype-environment
associations. Furthermore, the principal prey resource associated with this trait (i.e.,
zooplankton) can be examined in detail qualitatively and quantitatively both in the envi-
ronment and the predator diet. Such comparisons in natural settings are ideal to explore the
adaptive significance of the predator’s functional morphology. In their seminal paper,
Brooks and Dodson (1965) revealed that size selective predation of planktivorous fish
alters the species composition and reduces the body size of prey communities. This has
lead to a wide consensus that planktivorous fish regulates zooplankton communities (Zaret
1980; Lampert and Sommer 2007). When a proportion of fish population is adapting to
a zooplankton resource, the zooplankton community response by decreased body sizes
provides a feedback loop that further strengthen the selection pressure towards high for-
aging efficiency on small prey items. Such eco-evolutionary interactions have rarely been
addressed in relation to adaptive radiations of postglacial fish.
Here, we used a set of subarctic lakes that comprises a diversity gradient of coregonid
assemblages with increasing range and numbers of gill rakers, including (1) monomorphic
whitefish with ca. 20–30 gill rakers, (2) polymorphic whitefish populations with ca. 15–40
rakers, and (3) polymorphic whitefish and vendace, Coregonus albula (L.) with ca. 15–50
rakers). This range constitutes a natural setting to explore the role of increasing gill raker
numbers in zooplankton foraging, including the impact of coregonid radiation on zoo-
plankton prey communities. We assumed that foraging efficiency is associated with the
ability to utilize small prey, and predicted that zooplankton prey utilization is correlated to
the gill raker number. Furthermore, we predicted that zooplankton size, density and
community structure would change along the gradient from monomorphic to polymorphic
and finally to polymorphic whitefish and vendace lakes. Such a pattern would provide an
eco-evolutionary feedback mechanism where the prey community over evolutionary time
(e.g., under adaptive radiation) could shape the morphology of the predator.
Materials and methods
Study area and fish populations
We examined a set of eight northern Fennoscandian postglacial lakes situated in the
large subarctic Paatsjoki/Pasvik watercourse, including five Finnish (Lakes Aksuja
¨
rvi,
Vuontisja
¨
rvi, Vastusja
¨
rvi, Muddusja
¨
rvi and Paadar) and three Norwegian (Lakes Ellentj-
ern, Tjærebukta and Skrukkebukta) lakes (Fig. 1). This set of lakes represents a wide
gradient of coregonid populations. The Finnish headwater lakes discharge into the large
Lake Inarija
¨
rvi (hereafter L. Inari), whereas Norwegian lakes are situated in the lower
reaches of the watercourse (Fig. 1b). The study lakes are all oligotrophic (tot P 3–9 lgl
-1
,
Evol Ecol (2011) 25:573–588 575
123
tot N 145–240 lgl
-1
), well-oxygenated with neutral pH-values (6.8–7.2). Surface areas
range from 1 to 48 km
2
and maximum depths from 7 to 73 m (Table 1). The ice-free
season generally lasts from May–June to October–November. Coregonids, represented by
three different whitefish morphs and vendace, are the main zooplankton predators and the
dominant fish species (70–91% of numerical catches) in all lakes, except L. Ellentjern, but
the composition of the coregonid assemblage differs among the lakes.
The lakes were classified according to an increasing diversity of coregonids. Lakes
Aksuja
¨
rvi (hereafter L. Aksu), Ellentjern and Vuontisja
¨
rvi (L. Vuontis) were classified as
type 1, with only one whitefish morph present, the large sparsely rakered (LSR) morph.
LSR whitefish is identified and named according to body size and number of gill rakers,
which usually ranges from approx. 20–30 (Fig. 2). In lake type 2, LSR whitefish co-exist
with a densely rakered (DR) whitefish morph with approx. 30–40 gill rakers (L. Vastus) or
with DR whitefish and a small sparsely rakered (SSR) whitefish morph with approx. 15–20
gill rakers (Lakes Muddus and Paadar). In the most complex lake type 3 (Lakes Tjærebukta
and Skrukkebukta), polymorphic whitefish (LSR, DR and SSR whitefish morphs) co-exist
with vendace, which has the highest number of gill rakers (approx. 40–50) (Fig. 2).
Vendace is a pelagic zooplankton specialist (Helland et al. 2008) and does not occur
naturally in the Paatsjoki/Pasvik watercourse (Amundsen et al. 1999). Vendace was
introduced to L. Inari in the 1950–1960s and formed a very dense population during the
1980s leading to an invasion and colonization of the lower Paatsjoki lakes around 1990
(Amundsen et al. 1999). As a superior planktivore competitor over DR whitefish, vendace
has become the dominant fish species in the pelagic food web in many lakes in the lower
parts of the Paatsjoki/Pasvik watercourse (Bøhn and Amundsen 2001; Gjelland et al. 2007;
Bøhn et al. 2008).
Fish sampling
Sampling was conducted during September (years 2000–2007) in all the lakes. A long
sampling period was needed to include several lakes and coregonid populations from both
countries. This should not have any significant influence on the main patterns, since gill
Fig. 1 Map of (a) the northern Fennoscandia and (b) Paatsjoki/Pasvik watercourse. Study lakes with lake type
definition indicated in the parenthesis. 1 monomorphic whitefish, 2 polymorphic whitefish, 3 polymorphic
whitefish and vendace
576 Evol Ecol (2011) 25:573–588
123
Table 1 Background data on location, morphometry, water chemistry and fish fauna of the study lakes
Parameter Lake Aksu Lake Ellentjern Lake Vuontis Lake Vastus Lake Muddus Lake Paadar Lake Skrukkebukta Lake Tjærebukta
Lake type 1 1 1 2 2 2 3 3
Latitude (°N) 69°14
0
69°12
0
69°01
0
69°03
0
69°00
0
68°52
0
69°33
0
69°13
0
Longitude (°E) 26°53
0
29°06
0
27°04
0
27°07
0
26°50
0
26°35
0
30°07
0
29°11
0
Surface area (km
2
) 4 1 11 4 48 21 7 15
Altitude (m.a.s.l.) 206 71 151 146 146 144 21 52
Max depth (m) 10 7 31 15 73 56 38 30
Mean depth (m) 3.5 2.5 6.5 2.7 8.5* 11.7 14 4
Secchi depth (m) 2.5 4.5 8 2 3 6* 4–5.5 3–4.5
pH 6.9 7.2* 7.0 7.2* 7.1* 6.9 6.8
Tot P (lgl
-1
) 3 7* 7 5* 6* 7 9
Tot N (lgl
-1
) 165 170* 240 160* 160* 156 145
Coregonid
proportion (%)
81 39 90 70 86 91 85 78
Species/morphs
present
b, f, g, i, j,
k, l, m
b, g, i,
j, k, l
b, f, g, h, i,
j, k, l, m
a, b, f, g, h,
i, j, k, l, m
a, b, c, e, f,
g, h, i, j, k, l, m
a, b, c, f, g,
h, i, j, k, l, m
a, b, c, d, f,
g, i, j, k, l, m
a, b, c, d, f,
g, i, j, k, l, m
Coregonids and other fish species present in the study lakes are indicated with abbreviations. Lake type refers to the diversity of coregonid fish communities (1 monomorphic
whitefish, 2 polymorphic whitefish, 3 polymorphic whitefish and vendace)
* Data from Lapland Regional Environment Centre; a DR whitefish, b LSR whitefish, c SSR whitefish, d vendace, e Arctic charr, f grayling (Thymallus thymallus (L.),
g minnow (Phoxinus phoxinus (L.)), h three-spined stickleback, i nine-spined stickleback Pungitius pungitius (L.)), j perch (Perca fluviatilis L.), k pike (Esox lucius L.),
l burbot (Lota lota (L.)), m brown trout (Salmo trutta L.)
Evol Ecol (2011) 25:573–588 577
123
raker traits, habitat and diet selection of the studied coregonid populations are highly stable
among different years (Amundsen et al. 2004a, b; Kahilainen et al. 2004, 2007, 2009).
Coregonids were sampled from the three main habitats (littoral, pelagic and profundal)
using a combination of gill net series and pelagic trawling. The Finnish lakes were sampled
using a gill net set with eight nets, each having a length of 30 m and a height of 1.8 m, with
mesh sizes 12, 15, 20, 25, 30, 35, 45, and 60 mm from knot to knot. In addition, we used a
small pair trawl (5 m high, 8 m wide and cod-end mesh size 3 mm) in the pelagic zone of
these headwater lakes (see Kahilainen et al. 2004 for details). In the Norwegian lakes
coregonids were caught in the littoral and profundal habitats using benthic gill nets series
(length 40 m and height 1.5 m) with the mesh sizes of 10, 12.5, 15, 18.5, 22, 26, 35, and
45 mm, and in the pelagic using floating gill net series (length 40 m and height 6 m) with
mesh sizes of 8, 10, 12.5, 15, 18.5, 22, 26, and 35 mm.
Coregonids were field-identified to morph/species according to their overall habitus, head
shape and gill rakers (Amundsen et al. 2004b; Kahilainen and Østbye 2006). Minor overlap of
gill raker counts exist between the whitefish morphs, but these individuals can be classified
using combined information from body, head and gill rakers morphology. Uncertain SSR
whitefish can be defined from LSR whitefish due to its very peculiar habitus with large eye,
robust head, pronounced subterminal mouth and short bend gill rakers (Kahilainen and
Østbye 2006; Harrod et al. 2010). Uncertain DR whitefish was classified according to longer
gill rakers, terminal mouth and pointed head shape (Amundsen et al. 2004b; Harrod et al.
2010). Vendace can be separated from DR whitefish accurately as it has a characteristic
up-pointing protruding lower jaw, very pointed head, and very long and slender gill rakers.
The number of gill rakers was counted from the first left gill arch under a preparation
microscope. Stomachs were removed and prey items were identified as accurately as
possible. The relative contribution of each prey category was estimated (Amundsen et al.
1996). The coregonids diet consisted of pelagic zooplankton (mainly Bosmina spp.,
Daphnia spp., Holopedium gibberum, Calanoid and Cyclopoid copepods) and benthic
Fig. 2 Combined gill raker
distributions of whitefish morphs
(SSR small sparsely rakered,
LSR large sparsely rakered,
DR densely rakered) and vendace
in study lakes. Line illustrations
present the first left gill arch and
gill raker morphology of different
whitefish morphs
578 Evol Ecol (2011) 25:573–588
123
invertebrates (mainly molluscs, insect larvae and some benthic crustaceans). In the present
study, we focused on zooplankton prey, which is the only diet category considered here-
after. Body length of up to 30 individuals of undigested zooplankton was measured from
each stomach, when possible. In copepods, we measured the length from rostrum to furca
and in cladocerans from head to base of the tail spine (Kahilainen et al. 2005).
Zooplankton sampling
Zooplankton was sampled in September from the whole water column using two replicate
samples from each lake. In the Finnish lakes, samples were taken with a Limnos-tube (1 m,
volume 7.1 l) and zooplankton net (diameter 25 cm, mesh size 50 lm). Tube samples were
sieved through 50 lm zooplankton net and all samples were stored in 5% formalin solu-
tion. In the Norwegian lakes, samples were taken with a 30 l Schindler–Patalas trap or with
a vertically hauled zooplankton net (diameter 26 cm, mesh size 90 lm) and stored in 4%
formalin solution. Differences in sampling gears between countries may have effect on
zooplankton community results. The somewhat larger mesh size of zooplankton net and
higher volume of Schindler–Patalas trap used in Norwegian lakes could be more effective
to capture larger individuals as well as higher density and diversity of zooplankton com-
munity than the smaller gear used in Finnish side (Kalff 2002). We recognize this potential
bias in the interpretation of results and take this into account in prey size comparisons
among coregonids. However, the smallest zooplankton found in coregonid diet (0.30 mm,
Bøhn and Amundsen 1998) is substantially larger than the largest zooplankton net mesh
sizes used in this study (0.09 mm), ensuring that both sampling methods have captured
zooplankton sizes available to fish. Zooplankton samples were counted and measured in
the laboratory, excluding nauplii since they were not observed in the fish diet. The body
length of 30–50 randomly selected individuals from each zooplankton taxa (Bosmina,
Daphnia, Calanoid and Cyclopoid copepods) was measured. The average zooplankton
density per litre in the whole water column and the relative proportion of the main taxa
were calculated.
Statistical analyses
At the population level, the average number of gill rakers was compared with the proportion
of pelagic habitat use and diet as well as zooplankton prey size in the stomachs using
Spearman correlations. The same approach was used to explore potential correlations
between gill raker number and the proportion of pelagic diet and zooplankton prey size at the
individual level. In individual diet data, we calibrated datasets according to the lowest
samples sizes per morph/lake and then used random re-sampling for other morph/lake
combinations. Differences in zooplankton prey length data among morphs/species types
were harmonized by random re-sampling of 25 samples from a morphs/species within a lake
when available. This approach enabled separation of effects at the individual and population
levels. Differences in the zooplankton prey size among whitefish morphs and vendace were
tested with analysis of covariance (ANCOVA) using the zooplankton average length in each
lake as a covariate. The effect of individual gill raker number on median zooplankton prey
length in the stomach was tested with a general linear model (GLM) using gill raker number,
mean zooplankton length in the environment, and species/morph as predictor variables.
The effect of individual gill raker number on median zooplankton prey length was finally
tested with regressions within each species/morph on the full dataset, using prey length as the
response and gill raker number as the predictor variable.
Evol Ecol (2011) 25:573–588 579
123
A GLM was used to test for zooplankton size differences among lake types using
different zooplankton taxa and lake type as categorical variables. Analysis of variance
(ANOVA) was used to test for differences in the average zooplankton abundance (log
(x ? 1) transformed data) among lake types. The number of samples used for zooplankton
length measurements in coregonid stomachs and in the environment was different among
the lakes and we used bootstrapping for calibration of sample sizes before performing
ANCOVA, GLM and ANOVA. Subsequent pairwise comparisons in these analyses were
made with Tukey’s HSD tests.
Results
Strong positive correlations were found at the population level between the number of gill
rakers and both the pelagic habitat use (Fig. 3a, n = 19, Spearman correlation; r
s
= 0.83,
P \ 0.01) and the proportion of zooplankton in the diet (Fig. 3b, n = 19, r
s
= 0.84,
P \ 0.01). Polymorphic SSR and LSR whitefish populations with an average number of
gill rakers from 16–21 and 22–25, respectively, mainly used the benthic niche. Mono-
morphic LSR whitefish populations had an average number of gill rakers from 24 to 28 and
used both pelagic and benthic prey and habitat. DR whitefish had in average 33–35 gill
rakers and was the most pelagic and planktivorous whitefish morph. Vendace had on
average 43 gill rakers and was consistently a pelagic planktivore. In accordance with the
niche utilization, a significant negative correlation was observed between the average
number of gill rakers and zooplankton prey size (n = 19, r
s
=-0.83, P \ 0.01) (Fig. 3c).
The ANCOVA indicated that the average length of ingested zooplankton was dependent on
coregonid morph/species (F
3,187
= 91, P \ 0.001), but not on the observed average zoo-
plankton length in the pelagic environment (F
1,187
= 2, P = 0.13). The average length of
zooplankton prey gradually decreased from 1.90 mm in SSR whitefish, 0.95 mm in LSR,
0.61 mm in DR to 0.57 mm in vendace. These size differences in ingested prey were
different between all coregonid taxa (Tukey’s HSD tests, P \ 0.001), except between DR
whitefish and vendace (P = 0.978). At the individual level, the general patterns observed
at the population level were supported by a positive correlation between the number of gill
rakers and the proportion of zooplankton in diet (Fig. 4a, n = 48, r
s
= 0.68, P \ 0.01) and
Fig. 3 Correlations between gill raker number and (a) the proportion of pelagic habitat use, (b) the
proportion of zooplankton in the diet and (c) the zooplankton prey size at the population level. Population
types are marked with different labels: SSR whitefish (white circle), LSR whitefish (grey triangle), DR
whitefish (white square) and vendace (black diamond)
580 Evol Ecol (2011) 25:573–588
123
a negative correlation between number of gill rakers and zooplankton prey size (Fig. 4b,
n = 245, r
s
=-0.69, P \ 0.01). The GLM-analysis (adj. r
2
= 0.59) confirmed a strong
effect of morph/species on median zooplankton prey size (P \ 0.05 for all morphs/spe-
cies), and also indicated a negative effect of individual gill raker number within the morph/
species (P = 0.082). The regressions within each morph/species revealed that the negative
effect of individual gill raker number on zooplankton prey size was significant only within
the LSR and SSR whitefish (Table 2).
Fig. 4 Individual level
correlations between gill raker
number and (a) the proportion of
zooplankton in the diet and b the
average zooplankton prey size.
Population types are marked
with different labels:
SSR whitefish (white circle),
LSR whitefish (grey triangle),
DR whitefish (white square)
and vendace (black diamond)
Table 2 Results from the regression model prey length (in mm) = constant (a) ? gill raker number (Grn)
Species/morph aP(a) Grn P(Grn) Adj. r
2
P(overall) n
SSR 2.9 \0.001 -0.052 0.002 0.1 0.002 88
LSR 2.3 \0.002 -0.043 0.007 0.03 0.007 212
DR 0.23 0.46 0.011 0.24 0.001 0.24 331
Vendace 0.8 0.017 -0.007 0.22 0.18 0.22 6
Level of significance (P) is included for constant, gill raker number and overall model. Zooplankton length
in the environment was initially included in the models, but removed from all as it had no significant
contribution
Fig. 5 Zooplankton (a) body length, (b) density and (c) community composition along an increased diversity
gradient of coregonids (lake types: 1 monomorphic whitefish, 2 polymorphic whitefish, 3 polymorphic
whitefish and vendace). Zooplankton taxa indicated in bars are Bosmina spp. (white), Daphnia spp. (grey),
Holopedium gibberum (black), Calanoid (vertical hatching) and Cyclopoid copepods (diamond hatching).
In lake type 3, Daphnia spp. refers mainly to Daphnia cristata
Evol Ecol (2011) 25:573–588 581
123
There were distinct trends in the zooplankton community structure along the increasing
coregonid diversity gradient (Fig. 5). The average size of zooplankton differed among lake
types (GLM, F
2,1025
= 67, P \ 0.01) and gradually decreased from 0.65 mm in lake type
1, 0.60 mm in type 2 to 0.54 mm in lake type 3 (Tukey’s HSD tests, P \ 0.05) (Fig. 5a).
A sign of decreasing zooplankton abundance along the coregonid diversity gradient was
observed (Fig. 5b), but this was not statistically significant (ANOVA, F
2, 13
= 0.41,
P = 0.67). The average density in lake type 1 (8.2 ind l
-1
) tended to be higher than in lake
type 2 and 3 (5.4 and 5.8 ind l
-1
, respectively). Zooplankton community composition
changed from equal proportions of copepods and cladocerans in lake type 1 to a clear
dominance of cladocerans in lake type 3 (Fig. 5c). This was mainly due to a decrease in
the proportion of cyclopoid copepods and an increase in the proportion of Daphnia spp.,
in particular the small-sized and transparent species D. cristata, in lake type 3.
Discussion
We documented a strong relationship between gill raker numbers and the degree of
planktivory; a pattern that appears to be common in polymorphic fish populations in the
northern hemisphere (Schluter and McPhail 1992; Sku
´
lason et al. 1999; Amundsen et al.
2004a). The current study extended this common pattern to a much larger scale by includ-
ing all principal habitat types and a very wide range of gill raker number utilizing 19
different populations. There were strong positive correlations between predator trophic
morphology (gill rakers) and pelagic niche utilization (habitat and diet) as well as an
adaptive significance of increasing number of gill rakers facilitating the utilization of
smaller prey. The study furthermore extends the link between gill raker traits and niche
utilization from the commonly occurring littoral-pelagic morph pairs of various fish spe-
cies in the northern hemisphere (e.g., Schluter and McPhail 1993; Robinson and Parsons
2002), to also include the far less explored profundal niche. The fish with the lowest gill
raker numbers (\20) were almost exclusively associated with the profundal habitat, the
intermediate numbers (20–30) mainly with the littoral, whereas the highest numbers
(whitefish: 30–40; vendace [ 40) were associated with the pelagic habitat and a typical
zooplanktivore niche. These phenotype-environment correlations proved to be strong both
at the individual and population levels, suggesting that gill raker trait divergence is central
in adaptive radiation of whitefish between these three principal habitats of subarctic lakes.
The number of gill rakers is a single heritable trait in coregonid fishes (Sva
¨
rdson 1979;
Rogers and Bernatchez 2007), but apparently it also effectively captures much of other
morphological traits. Several trophic traits (i.e., head and body morphology) are associated
to fish feeding niche utilization along traditional pelagic-littoral resource axis in many
postglacial fish morphs (Schluter 1996; Robinson and Parsons 2002), but very little is
known about profundal adaptations. The SSR whitefish typically residing in the profundal
habitat, has the lowest gill raker counts among the explored whitefish morphs and a body
and head morphology that likely have an adaptive value in profundal foraging (Kahilainen
and Østbye 2006). Similar adaptations in trophic related traits were shown to be heritable
in a profundal Arctic charr (Salvelinus alpinus (L.)) morph specializing on soft bottom
benthos (Klemetsen et al. 2002; Knudsen et al. 2006). Foraging on prey items buried in soft
bottom profundal sediments requires some suction of mud (Kahilainen et al. 2003). A low
number of short, widely spaced gill rakers is probably sufficient to retain typical profundal
prey types (i.e., Pisidium bivalves and chironomid larvae) while allowing the mud to be
disposed through the gillraker slits (Kahilainen and Østbye 2006). A dense gillraker
582 Evol Ecol (2011) 25:573–588
123
apparatus would in contrast likely be clogged by mud (Amundsen et al. 2004b). The SSR
whitefish mainly consumed relatively large-sized prey, suggesting a limited foraging
efficiency on zooplankton. The LSR whitefish morph has intermediate numbers, length and
spacing of gill rakers and subterminal mouth which likely facilitate benthic foraging
(Kahilainen and Østbye 2006; Harrod et al. 2010). LSR whitefish is apparently less effi-
cient in predation of small-sized zooplankton than the specialized planktivore DR whitefish
morph that has large number of long and dense gill rakers and a terminal mouth and slender
body shape (Kahilainen and Østbye 2006). These morphological traits of DR whitefish are
well suited for pelagic planktivores (Webb 1984) and are likely to have evolved in the
absence of resource competitors like ciscoes/vendace (Bernatchez 2004; Bøhn et al. 2008).
The differences between coregonids in gill raker apparatus can be compared to the
divergence of beak shape in birds, jaw shape in amphibians, mandible shape in bats or baleen
plates in whales which all facilitate the use of different dietary niches (Werth 2004; Pfennig
et al. 2006; Price 2008; Nogueira et al. 2009). In fish, there is a common trend of increasing
number of gill rakers from piscivores to benthivores and finally to planktivores (Gibson
1988; Langeland and Nøst 1995). Our results on Coregonus demonstrate a similar intra-
genus benthivore-planktivore trend in gill raker numbers. Our field data furthermore show a
negative correlation between the number of gill rakers and zooplankton prey size both at the
population and individual levels. Zooplankton prey is available in all principal lake habitats
(littoral, profundal and pelagic zones), providing an opportunity for planktivory for all
whitefish morphs. The gill raker apparatus functions as a crossflow filter that directs prey
particles towards the oesophagus (Sanderson et al. 2001), and explains why increasing
number of gill rakers facilitates the retention of smaller prey sizes. Previous studies failing to
find similar correlations between gill raker traits and prey size in salmonids (Seghers 1975;
Sandlund et al. 1987; Budy et al. 2005), may not have captured the essential range of trait
variation that is demonstrated among the coregonids in the present study.
The observed strong correlation between gill raker number and prey utilization at the
individual level suggests a significant role of gill rakers in individual foraging efficiency
that may promote disruptive selection. Adaptive evolution and divergence of trophic traits
are generally linked to unequal utilization efficiency of prey resources between individuals
(Knudsen et al. 2007; Arau
´
jo et al. 2008), which may ultimately lead to differences in
fitness and promote disruptive selection that may act in the formation of new morphs
(Rueffler et al. 2006). In a monomorphic three-spined stickleback (Gasterosteus aculeatus
L.) population, Bolnick and Lau (2008) found evidence for disruptive selection via
intraspecific competition, as individuals with high or low gill raker counts had higher
growth rates than individuals with intermediate gill raker numbers. In addition, if mating is
assortative between phenotypically and ecologically similar individuals, the disruptive
selection provides a pathway to population divergence into morphs (Snowberg and Bolnick
2008) and subsequently to speciation (Dieckmann and Doebeli 1999; Schluter 2000).
Monomorphic LSR whitefish with intermediate number of gill rakers is the most common
population type in northern Fennoscandia and probably represents the ancestral morpho-
type (Østbye et al. 2006), since allopatric SSR or DR whitefish populations have not been
found in the region (Lehtonen and Niemela
¨
1998; Amundsen et al. 2004b). During the
early colonization of these postglacial lakes, ecological opportunities have presumably
been high for specialization to each of the principal habitat types and their associated prey
communities. These three principal trophic niches may promote disruptive selection on gill
raker traits by constituting peaks in an adaptive landscape, where each whitefish morph has
adapted morphologically to utilize one of these peaks. Monomorphic LSR whitefish with
intermediate gill raker number use all the principal lake habitats foraging both on
Evol Ecol (2011) 25:573–588 583
123
zooplankton and benthic macroinvertebrates (Amundsen et al. 2004b; Kahilainen et al.
2007). In sympatry with other morphs (i.e., in polymorphic lakes) the LSR whitefish
prefers littoral macroinvertebrates, whereas the SSR whitefish utilizes profundal benthos
and DR whitefish zooplankton (Harrod et al. 2010). Interestingly, the effect of gill raker
number on zooplankton prey size was strongest in the SSR whitefish, weaker but still
significant in the LSR whitefish, and with no significant effect in the DR whitefish and
vendace. This suggests a directional selection towards increasing gillraker numbers for
SSR and LSR whitefish individuals that utilize a planktivorous niche, whereas there seems
to be little support for directional selection on increasing gill raker number in DR whitefish
or vendace in these lakes. Taken collectively, our results support a scenario where LSR
whitefish has diverged into SSR and DR whitefish morphs via disruptive selection
primarily acting on gill raker morphology and foraging abilities (Østbye et al. 2006).
The differences in zooplankton community structure among the three lake types suggest a
general importance of gill raker numbers in relation to planktivore predation. Although the
sampling was performed only in September, the previous seasonal open water datasets of
zooplankton and niche utilization of whitefish morphs and vendace support the observed
patterns in this study (Bøhn and Amundsen 1998, 2001; Kahilainen et al. 2004, 2005;
Gjelland et al. 2009). However, there is a need for winter sampling during ice cover when
zooplankton community is certainly different due to lack of cladocerans (Tolonen 1998) and
niche utilization of coregonids may also differ (Jurvelius and Marjoma
¨
ki 2008). In this study,
we found that zooplankton body size and density decreased with increasing coregonid
diversity, a pattern commonly observed in zooplankton communities when the number of
specialized planktivorous fish species increases (Nilsson and Pejler 1973; Post et al. 2008;
Amundsen et al. 2009). However, this pattern has previously not been connected to adaptive
radiation in postglacial fish. These zooplankton community patterns could have been even
stronger, if sampling gear had been identical. The vendace-whitefish lakes (lake type 3) were
sampled using larger zooplankton gear that may have increased the average length of zoo-
plankton. In lakes with only LSR whitefish present the competition for zooplankton resources
in the pelagic habitat is expected to be weak. Accordingly, we observed large body size, high
density and wide diversity of zooplankton in these lakes. In lakes including DR whitefish,
however, increased competition for zooplankton was indicated by reduced body size, density
and availability of zooplankton. Under such conditions, the frequency of planktivory in the
LSR whitefish is low (Amundsen et al. 2004b; Kahilainen et al. 2007). This trend was even
more pronounced in polymorphic lakes with vendace present as both the LSR and even the
DR whitefish morphs were forced to utilize the benthic food resources (Bøhn and Amundsen
2001; Bøhn et al. 2008). Hence, in each step of increased coregonid diversity, predation
efficiency for zooplankton increases and accordingly modifies the zooplankton community.
Subsequently, this reduces the opportunities of SSR and LSR whitefish morphs to utilize the
zooplanktivore dietary niche. We argue that this represents an eco-evolutionary process with
a feedback loop that reduces the formation of intermediate phenotypes (and hybrids), and
increases resource segregation among morphs. Similar feedback loops between predator
morphology and resources have been found in zooplanktivore alewife Alosa pseudoharengus
populations (Palkovacs and Post 2008, 2009) and in seed-feeding Geospiza finches (Grant
and Grant 2008). This process is able both to create and maintain polymorphism in various
ecosystems, and may over time lead to the formation of new species. Our data represent
empirical support for the early stages of this process in pristine and relatively young fish
communities. In a broader perspective, including the well known adaptive radiation in much
older systems (like e.g., the speciation of cichlids), a profound link between ecological and
evolutionary timescales is strongly indicated (see also Hairston et al. 2005).
584 Evol Ecol (2011) 25:573–588
123
In conclusion, our study demonstrates the adaptive significance of gill rakers in for-
aging: an increasing number of gill rakers facilitates the utilization of smaller prey and is
advantageous to planktivory, but at the same time disadvantageous to benthivory, in
particular to feeding in the profundal sediments (Fig. 6). Apparently, the three principal
lacustrine habitats represent adaptive peaks, promoting disruptive selection leading to gill
raker divergence and polymorphism. The phenotype-environment correlations between
gill raker number and pelagic niche utilization proved to be strong both at the indi-
vidual and population levels. Evidently, the coregonid gill raker divergence influ-
ences the zooplankton community structure and likely creates an eco-evolutionary
feedback loop maintaining and possibly strengthening the segregation of pelagic and
benthic morphs.
Acknowledgments The authors thank the Ministry of Agriculture and Forestry, Municipality of Inari,
Finnish Cultural Foundation, Ella and Georg Ehrnrooth Foundation, Otto A. Malm Foundation, Emil
Aaltonen Foundation, European Regional Developmental Fund (project A30205), The Norwegian Research
Council (NFR 186320/V40 and 183984/S30), Norwegian Directorate for Nature Management, The County
Governor of Finnmark and Pasvik Kraft AS for funding. We also acknowledge the field and laboratory work
by Aikio O., Antti-Poika P., Dalsbø L., Eloranta A., Helminen M., Johannesen K.S., Johansson K.,
Ja
¨
a
¨
skela
¨
inen P., Kervinen J., Lien C., Marttila J., Ma
¨
enpa
¨
a
¨
K., Niemisto
¨
J., Pennanen, M., Pohtila J.,
Salonen, M., Sa
´
ren, J., Solberg K.G., Tuomaala, A. and Vatanen S. Muddusja
¨
rvi Research Station kindly
provided facilities during the field sampling. We like to thank White E. and Antti-Poika P. for line
illustrations and Malinen T. for comments on manuscript.
Fig. 6 Ecomorphological gradient of studied coregonid populations. Whitefish morphs (SSR small sparsely
rakered, LSR large sparsely rakered, DR densely rakered) and vendace body shapes are illustrated with line
drawings. Normal distributions illustrate niche widths and accompanying text indicates main habitat, diet
and ecological classification of different coregonids. Lowest arrow indicates increasing morphological
specialization towards zooplanktivory
Evol Ecol (2011) 25:573–588 585
123
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... Trophic ontogeny is common among fishes as gape size increases with body size, and thereby larger fish can consume larger, higher trophic level prey (Sánchez-Hernández et al., 2019). For Cisco and other zooplanktivorous fishes, gill raker morphology is an additional determinant of the size of prey items consumed (Gibson, 1988;Kahilainen et al., 2011;Langeland & Nøst, 1995). It was long thought that gill rakers act as a basic sieve filtering out prey items based on body size (i.e., dead-end sieve) (Hessen et al., 1988). ...
... The gill rakers are a primary functional structure for Cisco (and other zooplanktivores) and influence the size of the prey that is retained for consumption. As inter-gill raker spacing increases with body size (Link & Hoff, 1998), the minimum size of retained prey increases with body size (Kahilainen et al., 2011;O'brien, 1987;Roesch et al., 2013). Our study found that trophic position increased steadily rather than in a step-like manner (Figure 2). ...
Article
Full-text available
Cisco (Coregonus artedi) are a widespread, cold‐water zooplanktivore native to North America. Although Cisco are generally referred to as an “obligate zooplanktivore,” there is some evidence that the species exhibits considerable variability in trophic niche. Here, we assessed how Cisco body size relates to trophic position, that is, trophic ontogeny. We analysed ¹³C and ¹⁵N isotopes from Cisco ranging from 127 to 271 mm in body length (n = 66) from Trout Lake, Vilas County, Wisconsin, USA. ¹⁵N isotopes showed smaller Cisco had a trophic position of ~3, which steadily increased to ~3.5 for larger Cisco. Further, ¹³C isotope signatures showed Cisco transitioned to be more pelagically reliant (lower ¹³C signatures). Using gillnet catch data, we found that larger Cisco were using deeper habitats than smaller Cisco. Our results support that Cisco have significant variability in trophic niche even though they are traditionally thought of as an obligate planktivore. Overall, we emphasize that researchers should be cautious when generalizing Cisco trophic function, particularly when considering the broader food web.
... In particular, an increase in gill raker number and length or a decrease in the space between gill rakers is associated with zooplankton retention or planktivory in salmonids and several other species (Amundsen et al., 2004;Castillo-Rivera et al., 1996;Gibson, 1988;Kahilainen et al., 2011;MacNeill & Brandt, 1990;Roesch et al., 2013;Wright et al., 1983). Furthermore, gill raker morphology-in particular gill raker number-is heritable in trout and other salmonids (Bernatchez, 2004;Foote et al., 1999;Funk et al., 2005;Hessen et al., 1988;Leary et al., 1985;Østbye et al., 2005), suggesting that plastic responses are unlikely to fully explain shifts in feeding morphology. ...
... Third, our conclusion that morphological shifts connote adaptive evolution requires that these shifts aid in the retention of small planktonic prey, which may increase foraging efficiency and fitness in alpine lakes. Although we are not aware of studies investigating planktivory and feeding morphology in cutthroat or golden trout, increased gill raker number and length have been associated with planktivory in lake trout (Salvelinus namaycush, Martin & Sandercock, 1967), and gill raker number has been linked to feeding efficiency in other salmonid species (Amundsen et al., 2004;Hessen et al., 1988;Kahilainen et al., 2011;Langeland & Nøst, 1995;Roesch et al., 2013). ...
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Eco-evolutionary interactions following ecosystem change provide critical insight into the ability of organisms to adapt to shifting resource landscapes. Here we explore evidence for the rapid parallel evolution of trout feeding morphology following eco-evolutionary interactions with zooplankton in alpine lakes stocked at different points in time in the Wind River Range (Wyoming, USA). In this system, trout predation has altered the zooplankton species community and driven a decrease in average zooplankton size. In some lakes that were stocked decades ago, we find shifts in gill raker traits consistent with the hypothesis that trout have rapidly adapted to exploit available smaller-bodied zooplankton more effectively. We explore this morphological response in multiple lake populations across two species of trout (cutthroat trout, Oncorhynchus clarkii; and golden trout Oncorhynchus aguabonita) and examine the impact of resource availability on morphological variation in gill raker number among lakes. Furthermore, we present genetic data to provide evidence that historically stocked cutthroat trout populations likely derive from multiple population sources, and incorporate variation from genomic relatedness in our exploration of environmental predictors of feeding morphology. These findings describe rapid adaptation and eco-evolutionary interactions in trout and document an evolutionary response to novel, contemporary ecosystem change.
... The observed habitat distributions of small sparsely rakered whitefish and large sparsely rakered whitefish are in line with the findings of other studies, with the former residing almost Table 1 footnote. exclusively in the profundal zone and the latter utilizing predominantly the littoral zone, but also profundal habitats (Bøhn et al., 2008;Kahilainen et al., 2011;Praebel et al., 2013). The diet of small sparsely rakered whitefish was accordingly dominated by typical profundal prey, including chironomid larvae, Megacyclops sp., and Pisidium sp. ...
... (Kahilainen et al., 2017), which was confirmed by the observed low δ 13 C and high δ 15 N values. The diet of large sparsely rakered whitefish in both lakes was dominated by typical littoral prey, as has been noted in previous studies (see Kahilainen et al., 2011;Kelly et al., 2022). Similarly, typical of littoral feeders (Post, 2002), the large sparsely rakered whitefish had higher δ 13 C levels relative to vendace and the other two whitefish morphs. ...
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Mercury (Hg) is a serious concern for aquatic ecosystems as it may biomagnify to harmful concentrations within food webs and consequently end up in humans that eat fish. However, the trophic transfer of mercury through the aquatic food web may be impacted by several factors related to network complexity and the ecology of the species present. The present study addresses the interplay between trophic ecology and mercury contamination in the fish communities of two lakes in a pollution-impacted subarctic watercourse, exploring the role of both horizontal (feeding habitat) and vertical (trophic position) food web characteristics as drivers for the Hg contamination in fish. The lakes are located in the upper and lower parts of the watercourse, with the lower site located closer to, and downstream from, the main pollution source. The lakes have complex fish communities dominated by coregonids (polymorphic whitefish and invasive vendace) and several piscivorous species. Analyses of habitat use, stomach contents, and stable isotope signatures (δ15 N, δ13 C) revealed similar food web structures in the two lakes except for a few differences chiefly related to ecological effects of the invasive vendace. The piscivores had higher Hg concentrations than invertebrate-feeding fish. Concentrations increased with size and age for the piscivores and vendace, whereas habitat differences were of minor importance. Most fish species showed significant differences in Hg concentrations between the lakes, the highest values typically found in the downstream site where the biomagnification rate also was higher. Hg levels in piscivorous fish included concentrations that exceed health authorization limits with possible negative implications for fishery and human consumption. Our findings accentuate the importance of acquiring detailed knowledge of the drivers that can magnify Hg concentrations in fish and how these may vary within and among aquatic systems, in order to provide a scientific basis for adequate management strategies. This article is protected by copyright. All rights reserved. Environ Toxicol Chem 2023;00:0-0. © 2023 SETAC.
... Burress et al. 2020;Ronco et al. 2021), gill raker arrangement and morphology (e.g. Kahilainen et al. 2011), the shape of the lower pharyngeal jaw bone (e.g. Burress 2016; Ronco et al. 2021), the dentition on the pharyngeal jaws (e.g. ...
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Fish biologists have long assumed a link between intestinal length and diet, and relative gut length or Zihler’s index are often used to classify species into trophic groups. This has been done for specific fish taxa or specific ecosystems, but not for a global fish dataset. Here, we assess these relationships across a dataset of 468 fish species (254 marine, 191 freshwater, and 23 that occupy both habitats) in relation to body mass and fish length. Herbivores had significantly relatively stouter bodies and longer intestines than omni- and faunivores. Among faunivores, corallivores had longer intestines than invertivores, with piscivores having the shortest. There were no detectable differences between herbivore groups, possibly due to insufficient understanding of herbivorous fish diets. We propose that reasons for long intestines in fish include (i) difficult-to-digest items that require a symbiotic microbiome, and (ii) the dilution of easily digestible compounds with indigestible material (e.g., sand, wood, exoskeleton). Intestinal indices differed significantly between dietary groups, but there was substantial group overlap. Counter-intuitively, in the largest dataset, marine species had significantly shorter intestines than freshwater fish. These results put fish together with mammals as vertebrate taxa with clear convergence in intestine length in association with trophic level, in contrast to reptiles and birds, even if the peculiar feeding ecology of herbivorous fish is probably more varied than that of mammalian herbivores. Supplementary Information The online version contains supplementary material available at 10.1007/s11160-024-09853-3.
... The number and size of the lateral and medial rows have been associated with microalgae consumption in fish in turbid waters and muddy environments (Bishop et al., 2022;Tran et al., 2022). Species with an average number of 16-24 gill rakers feed in the benthic niche, while species with more than 30 rakers feed pelagically (Kahilainen et al., 2011).The common carp has 20-29 gill rakers in the present study. This study shows that gill rakers filter suspended organisms such as plankton or microalgae. ...
Article
The study aimed to investigate the morphologic aspects of common carp's gill arch and gill rakers (Cyprinus carpio, Linnaeus, 1758), an omnivore and highest-produced aquaculture species. The study used 10 common carp (395.35 ± 45.06 g) grown entirely under aquaculture conditions. The fish tissues were fixed with Glutaraldehyde (2.5%) for scanning electron microscopy and with formalin (10%) for stereomicroscopic examination. In the SEM examination, two types of taste papillae (Type II and Type III) were observed in the pharyngeal mucosa. Microridge-like structures in the epithelial layer were found to have two forms. The study findings indicate a significant decrease in gill arch lengths from cranial to caudal and a significant increase in rakers per unit area, as determined through digital calliper measurements and stereomicroscopic examinations (p < 0.05). However, there was no significant difference in measurements of gill arches and raker numbers between the bilateral symmetry of the gill arches (p > 0.05). In conclusion, it was observed that the epithelial structure on the common carp gill arch contained two types of microridge-like structures: the gill arch length decreased from cranial to caudal, and the rake density on these arches increased caudally.
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Population genomics analysis holds great potential for informing conservation of endangered populations. We focused on a controversial case of European whitefish ( Coregonus spp.) populations. The endangered North Sea houting is the only coregonid fish that tolerates oceanic salinities and was previously considered a species ( C. oxyrhinchus ) distinct from European lake whitefish ( C. lavaretus ). However, no firm evidence for genetic‐based salinity adaptation has been available. Also, studies based on microsatellite and mitogenome data suggested surprisingly recent divergence (c. 2500 years bp) between houting and lake whitefish. These data types furthermore have provided no evidence for possible inbreeding. Finally, a controversial taxonomic revision recently classified all whitefish in the region as C. maraena , calling conservation priorities of houting into question. We used whole‐genome and ddRAD sequencing to analyse six lake whitefish populations and the only extant indigenous houting population. Demographic inference indicated post‐glacial expansion and divergence between lake whitefish and houting occurring not long after the Last Glaciation, implying deeper population histories than previous analyses. Runs of homozygosity analysis suggested not only high inbreeding ( F ROH up to 30.6%) in some freshwater populations but also F ROH up to 10.6% in the houting prompting conservation concerns. Finally, outlier scans provided evidence for adaptation to high salinities in the houting. Applying a framework for defining conservation units based on current and historical reproductive isolation and adaptive divergence led us to recommend that the houting be treated as a separate conservation unit regardless of species status. In total, the results underscore the potential of genomics to inform conservation practices, in this case clarifying conservation units and highlighting populations of concern.
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In this study, we analyzed nuclear DNA (nDNA) variation by means of genotyping-by-sequencing (GBS) of three disc-bearing and seven non-disc-bearing Garra tashanensis from the Tashan Cave in Iran to clarify their systematic and ecological relationships. We performed genetic differentiation, NeighborNet, Admixture, and principal component analyses on genomic data. Admixture and principal component analyses revealed clear genetic differentiation between disc-bearing and non-disc-bearing morphotypes, which was not detected by mtDNA markers in previous work. However, there was a non-disc-bearing individual that clustered with disc-bearing individuals. Based on the results of this study, the most parsimonious justification for coexistence of disc-bearing and non-disc-bearing forms of Garra in Tashan Cave is a combination of mechanisms similar to character release (intra-specific morphological diversification to exploit a wider range of habitats in the absence of competitors or predators) and relaxed selection (no more selective advantage for a previously advantageous trait as a result of ecological changes). The detected genetic structure may be an indication of reproductive isolation between the two groups. These data imply that the respective forms of the Tashan Cave barb could be a case of ongoing sympatric speciation, but also that disc form cannot be used as a taxonomic character for Tashan Cave barb forms.
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The proper delimitation of species plays an important role in taxonomy as well as in studies related to speciation. However, introgressive hybridization can confuse our ability to accurately construct phylogenetic relationships, particularly when two closely related species coexist and crossbreed. Studies have shown that Hemiculter leucisculus and H. tchangi coexist widely in the upper reaches of the Yangtze River, having similar life history and morphological characteristics, which may lead to the occurrence of hidden hybridization. However, natural hybridization has not been reported in the system. Here, we focus on the sympatric sister-species H. leucisculus and H. tchangi, using mitochondrial and nuclear loci to verify the occurrence of hybridization and introgression, and to explore the hybridization pattern and its evolutionary significance. Our results clearly revealed that H. leucisculus and H. tchangi showed extensive introgressive hybridization and provided evidence of ongoing hybridization. Genetic data showed that strength of the introgression varied by geographic locality, the number of hybrids shows a gradual increase from upstream to downstream, which is mainly influenced by the abundance of species. Morphological results displayed that hybrids did not exhibit the intermediate type, so it isn’t easy to distinguish hybrids through morphological and there were mismatching in morphological and genetic assignment results. The present study suggests that species boundaries are maintained in the face of ongoing introgression due to the differences in parental species. Our research will help to understand the role of interspecific gene flow in shaping species boundaries and provide insights to better understand closely related species interactions and to develop timely strategies regarding species conservation in the future.
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Objective Here we determine how traditional morphometrics (TM) compares with geometric morphometrics (GM) in discriminating among morphologies of four forms of ciscoes of the Coregonus artedi complex collected from Lake Huron. Methods One of the forms comprised two groups of the same deepwater cisco separated by capture depth, whereas the other three forms were shallow‐water ciscoes. Result Our three groups of shallow‐water ciscoes were better separated (3% vs. 19% overlap) in principle component analysis (PCA) with TM data than with GM data incorporating semilandmarks (evenly spaced nonhomologous landmarks used to bridge between widely separated homologous landmarks). Our two deepwater cisco groups, comprising a putatively single form collected from different depths, separated more in PCAs with GM data (33% overlap) than in PCAs with TM data (66% overlap), an anomaly caused by greater decompression of the swim bladder and deformation of the body wall in the group captured at greater depths. Separation of the two deepwater cisco groups captured at different depths was not affected by the removal of semilandmarks. Assignment of forms using canonical variate analysis accurately assigned 86% of individuals using TM data, 98% of individuals using GM data incorporating semilandmarks, and 100% of individuals using GM data without semilandmarks. However, we considered assignments from the same form of deepwater cisco into separate groups as misassignments resulting from different capture depths, which reduced the accuracy of assignments with GM data incorporating semilandmarks to 66%. Conclusion Our study implies that TM will continue to have an important role in morphological discrimination within Coregonus and other fishes similarly shaped.
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Hypothesis: The opportunity for inter-individual niche differences in contrasting resource environments can induce divergent natural selection in trophic morphology within single gene pools. Organisms: Arctic charr (Salvelinus alpinus) caught in the littoral and pelagic habitats of two neighbouring sub-arctic lakes. Field sites: Two post-glacial lakes (Fjellfrøsvatn and Lille Rostavatn, North Norway) of similar size and physical structures, but with different fish diversities (two and six species, respectively). Methods: Analysis and comparison of trophic niche (habitat and diet usage) and trophic morphology (body form and head structure) data from individual fish. Only immature charr 19-25 cm long were used to reduce the effects of allometric growth and secondary sex traits. Conclusions: The utilization of multiple resource types has facilitated incipient steps towards the evolution of polymorphism in one lake, but not in the other. In Fjellfrøsvatn, individual specializations in benthivore and planktivore diet niches are correlated with inter-individual morphological differentiation. In contrast, the Arctic charr in Lille Rostavatn were restricted to zooplanktivory, and distinct morphological diversification was absent. We conclude that the two lakes have dissimilar opportunities for individual niche specialization and evolution of polymorphism.
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The astounding breadth of diversity of life on earth intrigues and amazes many people, while the future of world biodiversity is a cause for widespread concern. Within the current context of global interest in biological diversity, this is a timely review of the most recent research into the evolutionary origins of biological diversity and the processes of speciation, from a stellar cast of contributors. Recent studies have discovered considerable genetic and morphological variation both between and within populations of the same species. Yet the relation between this intraspecific variation and the processes of speciation remains poorly understood. When, how, and why do new species arise? The chapters in this book explore the question of how variation arises within species; some emphasize the ecological and behavioural basis of differentiation; others argue for the role of natural selection in generating speciation. Several chapters focus on the important emerging links between sexual selection, sexual conflict, and population differentiation. The final chapters of the book take a broader perspective on the question, and explore the fossil record for data on the origination of species diversity - and extinctions - in the past. This book is a must-have for all researchers and graduate students in the biological sciences who want to be abreast of the latest thinking on the evolution of biological diversity.
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Elucidating the causes of population divergence and species diversity is a central issue in evolutionary biology. As for any scientific discipline, progress in this field will be best achieved if studies are embedded into a strong, predictive, theoretical framework. In this view, perhaps the most comprehensive concept available to evolutionary biologists is the ecological theory of adaptive radiation. Its central elements were formalized in the first half of the twentieth century by founders of the evolutionary synthesis and others, namely Huxley (1942), Mayr (1942), Lack (1947b), Dobzhansky (1951), and Simpson (1953). The theory holds that adaptive radiation, including both phenotypic divergence and speciation, is ultimately the outcome of divergent natural selection stemming from environmental and resource heterogeneity, as well as competitive interactions. Schluter (2000) has recently re-evaluated and extended this theory in the light of studies that have been conducted since its formulation. Overall, this synthesis of knowledge has supported the great utility of the ecological theory of adaptive radiation, which indeed makes it one of the most successful theories of evolution ever advanced (Schluter 2000).