Phylogeography of the Prickly Sculpin (Cottus Asper) in North‐Western North America Reveals Parallel Phenotypic Evolution Acro
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Journal of Biogeography (J. Biogeogr.) (2015) 42, 1626–1638 ORIGINAL Phylogeography of the prickly sculpin ARTICLE (Cottus asper) in north-western North America reveals parallel phenotypic evolution across multiple coastal–inland colonizations Stefan Dennenmoser1,2*, Arne W. Nolte2, Steven M. Vamosi1 and Sean M. Rogers1 1Department of Biological Sciences, University ABSTRACT of Calgary, Calgary AB T2N 1N4, Canada, Aim Glacial cycles during the Pleistocene may have frequently contributed to 2Max-Planck Institute for Evolutionary parallel evolution of phenotypes across independently evolving genetic lineages Biology, 24306 Pl€on, Germany associated with separate glacial refugia. Previous studies based on morphology suggested that the prickly sculpin (Cottus asper) survived the Last Glacial Maxi- mum (LGM) in southern coastal and inland refugia, favouring allopatric diver- gence between coastal and inland prickling phenotypes, which vary in the degree to which spine-like scales cover the body of the fish. Herein, we aimed to test whether parallel evolution across multiple genetic lineages rather than a single-lineage origin of highly prickled inland sculpins could serve as an expla- nation for the biogeographical distribution of prickling phenotypes. Location North-western North America, Southeast Alaska and Canada (British Columbia). Methods We used data from mitochondrial haplotypes and 19 microsatellite loci to identify distinct genetic lineages as a basis to interpret patterns of phe- notypic evolution. Results The occurrence of multiple mtDNA groups suggests that highly prick- led inland phenotypes comprise more than one genetic lineage. Both mtDNA and microsatellite data are consistent with post-glacial dispersal along the coast and repeated coastal to inland colonization events, as opposed to inland dis- persal of a single lineage from a southern refugium to northern regions. Main conclusions Our results suggest that highly prickled inland phenotypes evolved repeatedly following multiple inland colonization events, probably via coastal rivers. The prickly sculpin therefore provides an example of recent (post-glacial) parallel evolution, potentially facilitated by standing genetic varia- *Correspondence: Stefan Dennenmoser, tion already present in the ancestral coastal populations. Max-Planck Institute for Evolutionary Biology, € Keywords August Thienemann Str. 2, 24306 Plon, Cottus asper Germany. , fish, morphometrics, multiple colonization events, North Amer- E-mail: [email protected] ica, Pacific Northwest, parallel evolution, phylogeography, Pleistocene. creates unique opportunities to investigate evolutionary con- INTRODUCTION sequences of allopatric separation in glacial refugia, rapid The north-west of North America is characterized by a com- range expansions into recently deglaciated areas, and mixing plex geomorphological history associated with multifaceted of genetic lineages in zones of secondary contact (Shafer phylogeographical patterns largely shaped by repeated glacia- et al., 2010). Such investigations elucidate the relative impor- tions during the Pleistocene (c. 2.5 Ma–12,000 years ago; tance of historical and ecological effects on intraspecific geo- reviewed in Shafer et al., 2010). The increasing knowledge of graphical variation (Avise et al., 1987; Shikano et al., 2010), the post-glacial history of numerous taxa in this region and are therefore integral towards testing predictions about 1626 http://wileyonlinelibrary.com/journal/jbi ª 2015 John Wiley & Sons Ltd doi:10.1111/jbi.12527 Phylogeography reveals parallel evolution the adaptive divergence of local populations (Knowles, Phenotypic divergence between highly prickled inland scul- 2009). Ecological adaptation through natural selection can be pins and weakly prickled coastal sculpins has therefore been inferred when the repeated colonization of a new habitat interpreted as a consequence of allopatric divergence between across independently evolving genetic lineages results in par- coastal and inland glacial refugia, followed by northward dis- allel phenotypic evolution (Lu & Bernatchez, 1999; Schluter, persal during deglaciation (Krejsa, 1965; McPhail, 2007). 2000). However, recent studies have demonstrated that the However, assumptions about post-glacial dispersal routes genetic basis of parallel phenotypes may vary among popula- and phenotypic divergence of C. asper are based on the tra- tions, ranging from identical or different mutations in the ditional view that species persisted solely in glacial refugia same gene to mutations in different genes (Elmer & Meyer, south of the ice sheets (Hewitt, 2004). Meanwhile, phylogeo- 2011; Elmer et al., 2014). For example, historical differentia- graphical studies have increasingly revealed the existence of tion in standing genetic variation may lead to different more northern, cryptic glacial refugia (reviewed in Shafer genetic pathways causing parallel evolution across the distri- et al., 2010) that may have provided additional sources for bution range of a species (Prunier et al., 2012), and genetic allopatric divergence and post-glacial range expansions. Thus, introgression among divergent lineages could increase geo- highly prickled inland populations may have evolved in par- graphical variation of genomic architectures (Bernatchez allel across multiple glacial lineages originating from both et al., 2010), potentially favouring different genetic pathways southern and northern refugia. during the parallel evolution of a similar phenotype. There- Here, we use multi-locus data (mitochondrial DNA and fore, it is increasingly important to consider the historical microsatellites), as well as phenotypic data (prickling catego- context of parallel evolution and its underlying genetic basis ries, morphometrics), to elucidate the phylogeographical to better understand targets and mechanisms of natural context for the disjunct inland distribution of highly prickled selection. As mitochondrial DNA presents a biased view of phenotypes in the prickly sculpin. We aimed to distinguish demographic history and may not be selectively neutral between two main hypotheses. (Dowling et al., 2008), phylogeographical studies that use 1. Our first hypothesis is that highly prickled inland popula- both mitochondrial and nuclear DNA markers for investigat- tions originated from a single southern inland refugium, fol- ing the historical background of parallel phenotypes across lowed by post-glacial colonization of inland areas through the range of a species are needed. proglacial lakes temporarily connecting neighbouring water- The prickly sculpin, Cottus asper Richardson, 1836, is a sheds. Accordingly, a long glacial phase of allopatric diver- euryhaline fish species characterized by both amphidromous gence between coastal and inland populations should result and purely freshwater populations. Consistent phenotypic in pronounced coastal–inland differentiation in both genetic variants have been observed across a wide distributional and morphological data. A decrease of genetic diversity range between southern Alaska and California, representing towards northern latitudes would be expected if founder potentially diverse historical backgrounds (Krejsa, 1965; events characterized post-glacial colonization. McPhail, 2007). Post-glacial colonization of inland regions 2. Our second hypothesis is that highly prickled inland scul- has resulted in the predominance of a highly prickled pheno- pins evolved following colonization from multiple inland type characterized by a dense lateral coverage with spiny, and coastal refugia. In this case, highly prickled inland phe- scale-like epidermal structures (Krejsa, 1965). A heritable notypes should be associated with multiple genetic lineages genetic basis of prickling probably exists, because a major rather than a southern inland lineage. If inland groups do quantitative trait locus (QTL) that affects prickling has been not share a common glacial history of long-time coastal– found in the European sculpin, Cottus perifretum (Cheng, inland separation, morphological divergence between coastal 2013). Geographically disjunct distributions in prickling and inland groups is not expected to be strong. Under this intensity have been found in additional Cottus species in scenario, decreases in genetic diversity towards northern Europe and North America (Koli, 1969; Freyhof et al., 2005; regions are not necessarily expected, because of the presence McPhail, 2007), but we are not aware of any apparent of northern glacial refugia and admixture zones. phenotype–environment associations that would indicate a common adaptive function of prickling. MATERIALS AND METHODS Cottus asper is thought to have survived the Last Glacial Maximum (LGM) in two glacial refugia south of the ice Sample collection and DNA sequence amplification sheets: a coastal refugium located in the Chehalis River region (south of Puget Sound, Washington State, USA) and Prickly sculpins were sampled with baited minnow traps an inland refugium in the Columbia River system (British during spring and summer 2009 and 2010 from 29 sites in Columbia, Canada, and Washington State, USA) (McAllister British Columbia and one site in Alberta (Fig. 1). A total of & Lindsey, 1961; Krejsa, 1965). Accordingly, two northward 1053 sculpins were collected, euthanized with an overdose of post-glacial colonization routes have been proposed: (1) clove oil, and preserved in 95% ethanol. Additionally, 14 fin coastal along-shore dispersal through salt-tolerant