Characterizing neutral and adaptive genomic differentiation in a changing climate: The most northerly freshwater fish as a model

Abstract

Arctic freshwater ecosystems have been profoundly affected by climate change. Given that the Arctic charr ( Salvelinus alpinus ) is often the only fish species inhabiting these ecosystems, it represents a valuable model for studying the impacts of climate change on species life‐history diversity and adaptability. Using a genotyping‐by‐sequencing approach, we identified 5,976 neutral single nucleotide polymorphisms and found evidence for reduced gene flow between allopatric morphs from two high Arctic lakes, Linne'vatn ( Anadromous, Normal , and Dwarf ) and Ellasjøen ( Littoral and Pelagic ). Within each lake, the degree of genetic differentiation ranged from low ( Pelagic vs. Littoral ) to moderate ( Anadromous and Normal vs. Dwarf ). We identified 17 highly diagnostic, putatively adaptive SNPs that differentiated the allopatric morphs. Although we found no evidence for adaptive differences between morphs within Ellasjøen, we found evidence for moderate ( Anadromous vs. Normal ) to high genetic differentiation ( Anadromous and Normal vs. Dwarf ) among morphs within Linne'vatn based on two adaptive loci. As these freshwater ecosystems become more productive, the frequency of sympatric morphs in Ellasjøen will likely shift based on foraging opportunities, whereas the propensity to migrate may decrease in Linne'vatn, increasing the frequency of the Normal morph. The Dwarf charr was the most genetically distinct group. Identifying the biological basis for small body size should elucidate the potential for increased growth and subsequent interbreeding with sympatric morphs. Overall, neutral and adaptive genomic differentiation between allopatric and some sympatric morphs suggests that the response of Arctic charr to climate change will be variable across freshwater ecosystems.

Limited genetic parallelism underlies recent, repeated incipient speciation in geographically proximate populations of an Arctic fish (Salvelinus alpinus)

“…A comparison of the locations in which sympatric resident and anadromous Arctic Charr are and are not genetically distinct could yield insights into the ecological factors driving genetic differentiation. Significant genetic differences have been observed among resident and anadromous Arctic Charr in Labrador (this study and Salisbury et al., 2018), Greenland (Doenz et al., 2019) and Svalbard (O'Malley et al., 2019) but not Baffin Island (Moore et al., 2014). Distance to the ocean and the associated migratory fitness costs (Finstad & Hein, 2012) may play a role in favouring genetically distinct residents as Baffin Island sites were <1 km from the ocean (Loewen et al., 2010) whereas the Labrador sites were all >10 km from the ocean (Ramah ~ 10 km, Brooklyn ~ 35 km, Esker North ~ 78 km, as measured using Google Earth Pro [GEP]).…”

“…Distance to the ocean and the associated migratory fitness costs (Finstad & Hein, 2012) may play a role in favouring genetically distinct residents as Baffin Island sites were <1 km from the ocean (Loewen et al., 2010) whereas the Labrador sites were all >10 km from the ocean (Ramah ~ 10 km, Brooklyn ~ 35 km, Esker North ~ 78 km, as measured using Google Earth Pro [GEP]). However, genetically distinct morphs in Svalbard (O'Malley et al., 2019) were only ~2 km (measured with GEP) from the ocean. The small size of Ramah Lake (0.25 km 2 , measured with GEP) also suggests that lake size did not prevent the genetic differentiation of morphs in the similarly sized Baffin Island lakes (0.15–1.2 km 2 ) (Loewen et al., 2009).…”

“…Residents remain in freshwater their entire lives; they mature at a younger age and smaller size and also achieve a smaller lifetime length than the anadromous morph (Jonsson & Hindar, 1982; Jonsson & Jonsson, 2001; Rikardsen et al., 2004). While residency and anadromy have been thought to be primarily plastic traits in Arctic Charr (Jonsson & Jonsson, 2001; Moore et al., 2014; Nordeng, 1983) recent evidence based on neutral markers suggests that sympatric resident and anadromous morphs may be genetically differentiated (Doenz et al., 2019; O'Malley et al., 2019; Salisbury et al., 2018). Given that the anadromous morph forms the basis of economically and culturally important subsistence, recreational, and commercial fisheries often run by Indigenous peoples (Moore et al., 2013; Scott & Crossman, 1973) an understanding of the genetic contribution to Arctic Charr life history is essential for management and conservation.…”

Population structure and genomic evidence for local adaptation to freshwater and marine environments in anadromous Arctic Char (Salvelinus alpinus) throughout Nunavik, Québec, Canada

“…However, population structure in Hudson Bay appeared weaker, as there were signs of admixture between rivers within 100 km. As discussed earlier, other studies on Arctic Char have attributed low genetic differentiation over long distances to recent post-glaciation colonization events (Moore et al, 2013; O’Malley et al, 2019). However, lower salinity and a longer summer period in Hudson Bay could also lead to higher connectivity between estuaries.…”

Genomic data support management of anadromous Arctic Char fisheries in Nunavik by highlighting neutral and putatively adaptive genetic variation

“…However, population structure in Hudson Bay was weaker, as there were signs of admixture between rivers within 100 km of each other. Other studies have attributed low genetic differentiation over long distances to recent postglaciation colonization events (Delgado et al, 2019;Moore et al, 2013;O'Malley et al, 2019). Nonexclusively, lower salinity and a longer summer period in Hudson Bay could also lead to higher connectivity between estuaries.…”