Convergent evolutionary processes driven by foraging opportunity in two sympatric morph pairs of Arctic charr with contrasting post-glacial origins

bs_bs_banner Biological Journal of the Linnean Society, 2012, 106, 794–806. With 7 figures Convergent evolutionary processes driven by foraging opportunity in two sympatric morph pairs of Arctic charr with contrasting post-glacial origins 1 Scottish Centre for Ecology and the Natural Environment, University of Glasgow, Rowardennan, Glasgow G63 0AW, UK 2 Facultad de Ciencias, Universidad Autónoma del Estado de México, Instituto Literario no. 100 Colonia Centro, Toluca, CP50000, México 3 Marine Scotland Science, Faskally, Pitlochry, Perthshire PH16 5LB, UK 4 School of Biological Sciences, Medical Biology Centre, Queen’s University Belfast, 97 Lisburn Road, Belfast BT9 7BL, UK 5 Instituto de Investigaciones Oceanológicas, Universidad de Antofagasta, Avenida Angamos 601, Antofagasta, Chile Received 14 December 2011; revised 26 February 2012; accepted for publication 26 February 2012 bij_1906 794..806 The expression of two or more discrete phenotypes amongst individuals within a species (morphs) provides multiple modes upon which selection can act semi-independently, and thus may be an important stage in speciation. In the present study, we compared two sympatric morph systems aiming to address hypotheses related to their evolutionary origin. Arctic charr in sympatry in Loch Tay, Scotland, exhibit one of two discrete, alternative body size phenotypes at maturity (large or small body size). Arctic charr in Loch Awe segregate into two temporally segregated spawning groups (breeding in either spring or autumn). Mitochondrial DNA restriction fragment length polymorphism analysis showed that the morph pairs in both lakes comprise separate gene pools, although segregation of the Loch Awe morphs is more subtle than that of Loch Tay. We conclude that the Loch Awe morphs diverged in situ (within the lake), whereas Loch Tay morphs most likely arose through multiple invasions by different ancestral groups that segregated before post-glacial invasion (i.e. in allopatry). Both morph pairs showed clear trophic segregation between planktonic and benthic resources (measured by stable isotope analysis) but this was significantly less distinct in Loch Tay than in Loch Awe. By contrast, both inter-morph morphological and life-history differences were more subtle in Loch Awe than in Loch Tay. The strong ecological but relatively weak morphological and life-history divergence of the in situ derived morphs compared to morphs with allopatric origins indicates a strong link between early ecological and subsequent genetic divergence of sympatric origin emerging species pairs. The emergence of parallel specialisms despite distinct genetic origins of these morph pairs suggests that the effect of available foraging opportunities may be at least as important as genetic origin in structuring sympatric divergence in post-glacial fishes with high levels of phenotypic plasticity. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 794–806. ADDITIONAL KEYWORDS: alternative phenotypes – discrete morphological variation – ecological segregation – foraging specialism – speciation. INTRODUCTION Within a single species, individuals often express one of two or more possible phenotypes for a given trait. *Corresponding author. E-mail: 794 Where these expressed phenotypes are discrete (i.e. without intermediates), they have been variously referred to as morphs, ecotypes, ecomorphs, and polyphenisms. The exact definition of each of these terms differs, and has not been consistently applied in the literature and, according to some studies, depends © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 794–806 MONICA V. GARDUÑO-PAZ1,2, COLIN E. ADAMS1*, ERIC VERSPOOR3, DAVID KNOX3 and CHRIS HARROD4,5 CONTRASTING SYMPATRIC CHARR MORPHS discontinuity in body size, although they segregate into individuals that spawn in either spring or autumn (spring-spawning and autumn-spawning charr morphs, respectively) (Alexander & Adams, 2000; Kettle-White, 2001). We compare these two contrasting sympatric, morph pairs aiming to address six hypotheses related to their status and the evolutionary processes that led to their formation. These are that the morph pairs in each lake: (1) (2) (3) (4) represent genetically distinct units; show similar genetic origin; comprise ecologically distinct units; differ in functionally significant morphological characteristics; (5) exhibit different life-history traits; (6) show similar patterns of evolutionary divergence. MATERIAL AND METHODS STUDY AREAS AND SAMPLING Arctic charr were collected from Loch Tay, Perthshire which drains to the east (56°30′ N; 004°10′ W, 26.4 km2 area; 102 m maximum depth; Murray & Pullar, 1910) during the spawning season, in October 2006. Charr were also collected from Loch Awe, Argyll and Bute, which drains to the west (56°20′ N, 005°05′W; 38.5 km2 area; 93 m maximum depth; Murray & Pullar, 1910) during the spawning seasons for this population, between 8 and 15 November 2006 (autumn-spawning charr) and 21 and 26 February 2007 (spring-spawning charr). Sampling in Loch Awe was conducted at known spawning sites (56°22′21.1″N, 005°4′24.6″W; autumn) and (56°15′06.3″N, 005°16′24.1″W; spring). Arctic charr were collected at all sites using standard benthic Nordic mono-filament survey gill-nets (Jensen & Hesthagen, 1996). Nets were set on the bottom of the lake (maximum depth in the range 2–20 m) perpendicular to the shore and fished overnight. Collected specimens were killed immediately and taken to the laboratory within 3 h; each individual was photographed, measured (standard length ± 1 mm), weighed (±0.1 g) and their sex and maturity status determined. Otoliths were removed for age determination. The adipose fin was removed and preserved in 100% ethanol for genetic analysis. Allocation of charr to either the small or large body size morphs was determined (for sexually mature fish only) on the basis of body size only (Adams et al., 2003). Charr from Loch Awe were allocated to one of the alternative morphs only by the occurrence of sexual maturity at one of the two sampling periods. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 794–806 upon the underlying nature of the expressed phenotype (West-Eberhard, 1989). However, all definitions have one common attribute, a discontinuity in the spectrum of expressed phenotypes for a given trait (i.e. expression of discrete, alternative phenotypes) (Garduno-Paz & Adams, 2010). The expression of two or more discrete phenotypes allows multiple, alternative modes upon which selection can act semiindependently, providing a basis for the divergence of alternative phenotypes towards different evolutionary outcomes (West-Eberhard, 2003). This effect is particularly evident where alternative phenotypes are expressed in sympatry (Schluter & McPhail, 1992) and where the expressed phenotypes have a (...truncated)