Phylogeography of the prickly sculpin (Cottus asper) in north‐western North America reveals parallel phenotypic evolution across multiple coastal–inland colonizations

Abstract

Aim Glacial cycles during the Pleistocene may have frequently contributed to parallel evolution of phenotypes across independently evolving genetic lineages associated with separate glacial refugia. Previous studies based on morphology suggested that the prickly sculpin (Cottus asper) survived the Last Glacial Maximum (LGM) in southern coastal and inland refugia, favouring allopatric divergence 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 explanation 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 phenotypic evolution. Results The occurrence of multiple mtDNA groups suggests that highly prickled 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 dispersal 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 variation already present in the ancestral coastal populations.

Adaptive genomic divergence under high gene flow between freshwater and brackish‐water ecotypes of prickly sculpin (Cottus asper) revealed by Pool‐Seq

“…Divergent life history ecotypes have presumably evolved from standing genetic variation of the same genetic lineage following deglaciation around 14 000 years ago (Dennenmoser et al . ). Independence of environmental and genetic distance from geographic distance implies that the patterns of differentiation of C. asper are shaped by ongoing gene flow (Dennenmoser et al .…”

“…In C. asper , divergent life history ecotypes occupying brackish‐water and freshwater niches were presumably established following the colonization of coastal river systems after the last glacial maximum around 14 000 years BP (Dennenmoser et al . ), thus presenting a suitable study system for investigating the early stage of genomic divergence in the presence of gene flow.…”

“…Similarly, differentiation among freshwater and brackish-water groups in the presence of gene flow is known from other euryhaline teleosts such as Atlantic killifish (Fundulus heteroclitus), European whitefish (Coregonus lavaretus) and threespine stickleback (Gasterosteus aculeatus), in which numerous adaptive candidate genes for salinity tolerance have been characterized (Whitehead et al 2011Jones et al 2012a, b;Papakostas et al 2012). In C. asper, divergent life history ecotypes occupying brackish-water and freshwater niches were presumably established following the colonization of coastal river systems after the last glacial maximum around 14 000 years BP (Dennenmoser et al 2015), thus presenting a suitable study system for investigating the early stage of genomic divergence in the presence of gene flow.…”

Drift effects on the multivariate floral phenotype ofCalceolaria polyrhizaduring a post‐glacial expansion in Patagonia

“…Although Quaternary environmental changes substantially impacted the landscape and promoted fast evolutionary changes in numerous species (Hewitt, 2000;Tribsch & Sch€ onswetter, 2003;Hosner et al, 2014), the connection between phylogeography and phenotypic evolution has been little examined in animal systems (e.g. Diniz-Filho et al, 1999;Kuriyama et al, 2011;Dennenmoser et al, 2015) and almost unexplored in plants. To our knowledge, the present study is the first that explores the geographical variation in the variance-covariance matrices under an explicit phylogeographic scenario.…”

Intraguild predation leads to genetically based character shifts in the threespine stickleback

“…A subset of these lakes was also colonized by prickly sculpin ( Cottus asper ), a freshwater teleost fish and IG‐predator of the threespine stickleback (Dennenmoser et al. ). Sculpin grow to larger size than stickleback and consume juvenile and adult stickleback up to 60% of their body length (McPhail ; Reimchen ).…”