Divergent functional traits in three sympatric Arctic charr Salvelinus alpinus morphs are not coupled with the age of the lineage divergence

Hydrobiologia DOI 10.1007/s10750-016-2964-7 CHARR II Divergent functional traits in three sympatric Arctic charr Salvelinus alpinus morphs are not coupled with the age of the lineage divergence Carolyn Bryce . Alicia Fraser . Rune Knudsen . Ron Greer . Colin Adams Received: 5 March 2016 / Revised: 21 August 2016 / Accepted: 22 August 2016 Ó The Author(s) 2016. This article is published with open access at Springerlink.com Abstract Three genetically discrete morphs of Arctic charr in Loch Rannoch, Scotland originated from a recent divergence within the lake (in situ) (piscivore and benthivore morphs) and from secondary contact of two older lineages (ex situ; a planktivore–piscivore/ benthivore divergence). To test if the expression of traits with strong functional roles was linked to the age of the divergence, fin and gill anatomy, and dentition were quantified and compared across morphs. Five additional working hypotheses suggesting a rank order of trait expression amongst morphs were also tested. The planktivorous morph had more rays in the dorsal and pectoral fins, longer gill rakers (but not more) as well as a smaller gill cavity than the other two morphs. Guest editors: M. Power, R. Knudsen, C. Adams, M. J. Hansen, J. B. Dempson, M. Jobling & M. Ferguson / Advances in Charr Ecology and Evolution C. Bryce  A. Fraser  C. Adams (&) The Scottish Centre for Ecology & the Natural Environment, Institute of Biodiversity, Animal Health and Comparative Medicine, CMVLS, University of Glasgow, Rowardennan, Glasgow G63 0AW, UK e-mail: R. Knudsen  C. Adams Department of Arctic and Marine Biology, UiT The Arctic University of Norway, 9037 Tromsö, Norway R. Greer The Armoury House, Blair Atholl, Perthshire PH18 5SG, UK The piscivorous morph had more palatine teeth and longer teeth on the mandible, pre-maxillary and glossohyal bones, and a larger buccal cavity. These differences indicate a differential response to selection in these functional anatomical features most likely related to morph foraging specialisms. Notably, between-morph divergences in the expression of these traits were not simply linked to the length of divergence between morphs and have arisen equally quickly in the recent (in situ) divergence as they have in older, ex situ divergences. Keywords Evolution  Trophic specialism  Ecomorphs  Phenotypic variation Introduction The extent to which species exhibit intra-specific structuring in their genotype and expressed phenotype is becoming increasingly apparent (see e.g. Kang et al., 2013; Swislocka et al., 2013). In some systems, it is clear that such structuring has arisen quickly and relatively recently (Gislason et al., 1999; Garduño-Paz et al., 2012). This is particularly true for fishes occupying freshwater lakes that have been recently glaciated (see Skulason et al., 1999 for a general overview; for contrasting exemplars, see Ferguson, 1989; Svanbäck & Eklöv, 2004; Verspoor et al., 2005; Hendry et al., 2009; Muir et al., 2015). 123 Hydrobiologia Where such patterning has been reported, it is often inferred, although difficult to empirically demonstrate, that this is the result of a local adaptive response to local selection pressures which are either contemporary or the result of a legacy of historical selection (Bush & Adams, 2007; Garant et al., 2007; Woods et al., 2012). Patterns exhibited by such structuring are highly informative in that they provide insights into the evolutionary processes that have ultimately shaped phenotypic and genetic configurations in nature. Such insights are even more valuable where structuring has developed in a single population and has manifested as distinct intra-specific groups occupying the same ecosystem. In such systems, the observed evolutionary divergences are maintained and driven in populations of individuals exposed to broadly the same environmental conditions (temperature, latitude, foraging opportunities, biotic, competition, etc.). Several species of freshwater fishes inhabiting recently glaciated lakes show clear and distinct structuring of phenotype in sympatry. Phenotypic structuring is often also reflected in genotype differences. See as exemplars, European whitefish, Coregonus lavaretus (L. 1758) (Kahilainen & Ostbye, 2006; Siwertsson et al., 2013), pygmy whitefish, Prosopium coulterii (Eigenmann & Eigenmann 1892) (Gowell et al., 2012), North American lake whitefish, Coregonus clupeaformis, Lacepede 1803, (Gagnaire et al., 2013), both three-spined stickleback, Gasterosteus aculeatus L. 1758, (Lavin & McPhail, 1986; Defaveri et al., 2013), and nine-spined stickleback, Pungitius pungitius (L. 1758) (Ishikawa et al., 2013) and European perch, Perca fluviatilis L. 1758, (Svanbäck & Persson, 2004). Where this occurs, there is almost always a strong ecological divergence between the alternative groups, most often manifested as alternative foraging specialisms. This is usually accompanied by some morphological adaptations related to the foraging specialisation. Where at least the ecological and morphological divergences amongst groups are clear and discrete, the alternative phenotypes are often termed morphs or ecomorphs. Prominent amongst the species known to exhibit multiple morphs living in sympatry is the Arctic charr, Salvelinus alpinus (L. 1758) (Danzmann et al., 1991; Fraser et al., 1998; Jonsson & Jonsson, 2001; Klemetsen et al., 2003; Knudsen et al., 2007). In some lakes where such polymorphisms have been described, 123 the morphs have arisen in sympatry (Gislason et al., 1999; Verspoor et al., 2010; Garduño-Paz et al., 2012), but this is not always be the case (see Garduño-Paz et al, 2012). There is significant evidence from Arctic charr of parallel, in situ divergences resulting in the emergence of similar ecological specialists occurring in different lake systems across the range of the species (Jonsson & Jonsson, 2001; Alekseyev et al., 2002; Adams et al., 2008). There is a general assumption that phenotypic differences exhibited by sympatric morphs are adaptive, driven by selection forces and are thus strongly functional. The vast majority of analyses of phenotype in Arctic charr have focused on external morphology (Adams & Huntingford, 2002a), but there are a number of other elements of fish anatomy which have important ecological functions which are poorly understood. Gill raker length and spacing are frequently correlated with foraging specialisms in fishes. Fish exhibiting closely spaced and longer rakers often show evidence of foraging on smaller prey than conspecifics, or closely related species, with the alternative gill raker format (for a thorough review see Gerking, 1994). Gill raker number in Arctic charr has been shown to vary between morphs (Frost, 1965), but the evidence of the literature is that they do not vary as obviously as they do in ecomorphs of related fish groups, for example, amongst the coregonidae (Kahilainen et al., 2011). The dentition of closely re (...truncated)