Rapid parallel adaptive radiations from a single hybridogenic ancestral population

Abstract

The Alpine lake whitefish (Coregonus lavaretus) species complex is a classic example of a recent radiation, associated with colonization of the Alpine lakes following the glacial retreat (less than 15 kyr BP). They have formed a unique array of endemic lake flocks, each with one to six described sympatric species differing in morphology, diet and reproductive ecology. Here, we present a genomic investigation of the relationships between and within the lake flocks. Comparing the signal between over 1000 AFLP loci and mitochondrial control region sequence data, we use phylogenetic tree-based and population genetic methods to reconstruct the phylogenetic history of the group and to delineate the principal centres of genetic diversity within the radiation. We find significant cytonuclear discordance showing that the genomically monophyletic Alpine whitefish clade arose from a hybrid swarm of at least two glacial refugial lineages. Within this radiation, we find seven extant genetic clusters centred on seven lake systems. Most interestingly, we find evidence of sympatric speciation within and parallel evolution of equivalent phenotypes among these lake systems. However, we also find the genetic signature of human-mediated gene flow and diversity loss within many lakes, highlighting the fragility of recent radiations.

Managing cryptic biodiversity: Fine‐scale intralacustrine speciation along a benthic gradient in Alpine whitefish (Coregonusspp.)

“…sp. “Alpnacherfelchen” (“ Alpnach ”), appears to be restricted to a separate sub‐basin of Lake Lucerne, Lake Alpnach (Hudson et al., 2011; Svarvar & Müller, 1982). More research is required to establish the ecological and evolutionary distinctness of the latter taxon from other Lucerne whitefish.…”

“…Indeed, several lines of evidence support an ecological speciation scenario via the action of divergent natural selection for the origin of Lake Lucerne whitefish: (i) our study confirms previous works (Douglas, Brunner, & Bernatchez, 1999; Hudson et al., 2011) in showing that similar ecomorphs have arisen repeatedly across different lake flocks in the Alpine whitefish radiation. (ii) Significant structuring of neutral genetic and adaptive phenotypic variation was observed along an ecological gradient (water depth), whereas nonsignificant isolation‐by‐distance was uncovered between spatially distant but phenotypically similar populations within Lake Lucerne, strong evidence for the primacy of selective rather than neutral processes in the generation of intralacustrine whitefish diversity.…”

“…Douglas and Brunner (2002) include a population from Lake Lucerne labelled only as “Blaufelchen.” This population groups closest in their study to Lake Constance taxa and another taxon of recognized allochthonous origin, C . fatioi from Lake Thun (Hudson et al., 2011). Blaufelchen is the local name for C. wartmanni , an intermediate‐sized whitefish endemic to Lake Constance, with relatively high gill‐raker counts (mean = 34.5; Vonlanthen et al., 2012).…”

“…Around 30 species of whitefish in the larger subalpine lakes of Switzerland have arisen following the glacial retreat ~15,000 years BP (Hudson et al., 2011; Steinmann, 1950; Vonlanthen et al., 2012). These lakes are characterized by high levels of endemicity in their whitefish fauna.…”

“…While this supplemental stocking may have helped maintain some native whitefish species experiencing anthropogenic eutrophication in the mid‐to‐late 20th century, overall stocking has negatively impacted endemic diversity. This negative impact has occurred both through the translocation of non‐native whitefish species among lakes and through increased interspecific gene flow via uncontrolled crossing when carrying out supportive breeding (Eckmann, 2012; Hirsch et al., 2013; Hudson et al., 2011). Many of the Alpine lakes harbouring whitefish radiations have recovered from eutrophication (Vonlanthen et al., 2012); however, uncontrolled supportive breeding is still routinely carried out.…”