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The role of gill raker number variability in adaptive radiation of coregonid
fish
Kimmo K. Kahilainen
1,2*
, Anna Siwertsson
3
, Karl Ø. Gjelland
3
, Rune Knudsen
3
,
Thomas Bøhn
3,4
and Per-Arne Amundsen
3
1
Department of Environmental Sciences, University of Helsinki, P.O. Box 65, FI-00014
Finland,
2
current address: Kilpisjärvi Biological Station, University of Helsinki,
Käsivarrentie 14622, FI-99490 Kilpisjärvi, Finland
3
Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and
Economics, University of Tromsø, N-9037 Tromsø, Norway
4
GenØk – Centre for Biosafety, The Science Park, P.O. Box 6418, N-9294 Tromsø, Norway
* Author for correspondence (kimmo.kahilainen@helsinki.fi)
Running title: Gill rakers and adaptive radiation of coregonid fish
Keywords: ecological speciation, foraging trait, polymorphism, vendace, whitefish morphs
Total word count (excluding references, tables and figures): 5401 words
Abstract: 202 words
Introduction: 1047 words
Materials and methods: 1513 words
Results: 515 words
Discussion: 1836 words
Acknowledgments: 137 words
Number of references: 73
Number of tables and figures: 8
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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 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.
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INTRODUCTION
In adaptive radiation, a common ancestor is diverged into two or more species via ecological
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 (Dieckmann 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 (Svärdson 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
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al 2006; Hudson et al 2007). Different morphs of coregonids have traditionally been
identified from the number of gill rakers (Svärdson 1952; Lindsey 1981; Bernatchez 2004)
which is a heritable and ecologically important trait (Svärdson 1979; Rogers and Bernatchez
2007). The European whitefish (Coregonus lavaretus (L.)) is the most diverse coregonid
species, and have 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 suggesting
parallel evolution within each lake (Østbye et al 2006). 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 utilization 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).
The trophic role of the gill raker apparatus is related to prey retention efficiency, where the
gill rakers function as a cross-flow filter forcing the prey items towards the oesophagus of the
fish (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
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possibilities of small prey, further improving the foraging efficiency. However, a dense
gillraker apparatus 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
than e.g. feeding on small-sized zooplankton. 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). Coregonids 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 environment 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 foraging 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
