Genetic population structure in prickly sculpin (Cottus asper) reflects isolation-by-environment between two life-history ecotypes

Abstract

Life-history transitions have evolved repeatedly in numerous taxa, although the ecological and evolutionary conditions favouring such transitions in the presence of gene flow remain poorly understood. The present study aimed to disentangle the effects of isolation-by-distance and isolation-by-environment on genetic differentiation between two sympatric life-history ecotypes. Using 14 microsatellite loci, we first characterized amphidromous and freshwater groups of Cottus asper in a high gene flow setting in the Lower Fraser River system (south-western British Columbia, Canada) to test for the effects of habitat and geographical distance on the distribution of life-history ecotypes. Within the main river channel, no genetic differentiation was found, whereas tributaries even close to the estuary were genetically differentiated. Partial mantel tests confirmed that genetic differentiation between river tributaries and the main channel was independent from geographical distance, with distance-scaled migration rates indicating reduced gene flow from the main channel into the tributaries. Our results suggest that isolation-by-environment can play an important role for the early stage of life-history transitions, and may promote differentiation among life-history ecotypes despite the presence of gene flo

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

“…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 . ). Accordingly, ongoing genetic exchange coupled with large population sizes of C. asper should reduce the influence of genetic drift and enhance signals of natural selection on beneficial allelic variants.…”

“…This interpretation is consistent with previous estimates of reduced migration from estuarine into tributary freshwater sites (Dennenmoser et al . ). Currently, we do not know whether osmoregulatory divergence alone could be strong enough to reduce gene flow among freshwater and brackish‐water habitats.…”

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

“…However, the lack of shared haplotypes among southern and northern inland regions does not support far northward dispersal of southern inland haplotypes. Gene flow among coastal populations of C. asper is facilitated by a high dispersal capability of salt‐tolerant, planktonic larval stages (Krejsa, ; McPhail, ), which is well known from many amphidromous species including sculpins (Whiteley et al ., ; Dennenmoser et al ., ). Accordingly, secondary contact between coastal northern and southern genetic lineages may have contributed to the occurrence of elevated genetic diversities and the admixture of haplotypes in Auke Creek (Southeast Alaska) and Bella Coola River (central BC).…”

Genomic footprints of adaptation in a cooperatively breeding tropical bird across a vegetation gradient

“…Heterogeneous landscapes can increase genetic differentiation by affecting gene flow between populations, regardless of geographic distance (Foll & Gaggiotti, ; Nosil, Vines, & Funk, ; Thorpe, Surget‐Groba, & Johansson, ; Wang & Bradburd, ). This IBE pattern is thought to be generated by local adaptation (Bradburd, Ralph, & Coop, ; Wang & Bradburd, ; Wang & Summers, ), especially under strong selective regimes that constrain dispersal and affect mating synchrony along an environmental gradient (Dennenmoser, Rogers, & Vamosi, ; Mendez, Rosenbaum, Subramaniam, Yackulic, & Bordino, ; Nielsen et al., ; Saint‐Laurent, Legault, & Bernatchez, ; Schweizer et al., ; Sexton, Hangartner, & Hoffmann, ). This effect is, however, controversial because gene flow is thought to stall local adaptation (Bridle, Polechová, Kawata, & Butlin, ; Haldane, ; Wright, ), implying that IBD patterns may be more common in nature (Meirmans, ; Slatkin, ; Wang, Glor, & Losos, ).…”

“…This effect is, however, controversial because gene flow is thought to stall local adaptation (Bridle, Polechová, Kawata, & Butlin, ; Haldane, ; Wright, ), implying that IBD patterns may be more common in nature (Meirmans, ; Slatkin, ; Wang, Glor, & Losos, ). However, IBE has become a likely explanation for population genetic differences in many taxa and environmental frameworks, including some orchids (Mallet, Martos, Blambert, Pailler, & Humeau, ), fish (Dennenmoser et al., ), birds (Manthey & Moyle, ) and mammals (Lonsinger, Schweizer, Pollinger, Wayne, & Roemer, ; Mendez et al., ), which suggests that IBE is also frequently found in nature. Disentangling the relative effects of IBD and IBE is thus essential to understanding the ecology of local adaptation and phenotypic evolution (Bradburd et al., ; Sexton et al., ; Wang & Bradburd, ; Wang et al., ).…”