Rapid buildup of sympatric species diversity in Alpine whitefish

Abstract

Adaptive radiations in postglacial fish offer excellent settings to study the evolutionary mechanisms involved in the rapid buildup of sympatric species diversity from a single lineage. Here, we address this by exploring the genetic and ecological structure of the largest Alpine whitefish radiation known, that of Lakes Brienz and Thun, using microsatellite data of more than 2000 whitefish caught during extensive species‐targeted and habitat‐randomized fishing campaigns. We find six strongly genetically and ecologically differentiated species, four of which occur in both lakes, and one of which was previously unknown. These four exhibit clines of genetic differentiation that are paralleled in clines of eco‐morphological and reproductive niche differentiation, consistent with models of sympatric ecological speciation along environmental gradients. In Lake Thun, we find two additional species, a profundal specialist and a species introduced in the 1930s from another Alpine whitefish radiation. Strong genetic differentiation between this introduced species and all native species of Lake Thun suggests that reproductive isolation can evolve among allopatric whitefish species within 15,000 years and persist in secondary sympatry. Consistent with speciation theory, we find stronger correlations between genetic and ecological differentiation for sympatrically than for allopatrically evolved species.

Allopatric and sympatric diversification within roach (Rutilus rutilus) of large pre‐alpine lakes

“…Roach represent an ideal candidate to test for intraspecific diversification, given: (a) its broad dietary niche providing the ecological opportunity to explore a wide range of the available niche space and thus to potentially adapt to one or more niches, (b) its wide distribution across Europe (Kottelat & Freyhof, ), (b) its ability to inhabit an array of different environments (including streams and the pelagic and littoral zones of lakes (Svanbäck et al., ; Faulks et al., ), (d) its large population sizes, and (e) its modest economic importance, resulting in little to no direct management. Additionally, the roach in this study (Figure ) often coexist with adaptive radiations of whitefish and are ecologically similar to some of the shallow water whitefish species (Doenz, Bittner, Vonlanthen, Wagner, & Seehausen, ; Hudson, Vonlanthen, & Seehausen, ; Vonlanthen et al., ), thus providing the potential for ecological niche shifts of roach in response to interspecific interactions, as has been shown for other fish species (Braband, ; Faulks et al., ; Persson, ).…”

“…The slight differentiation of roach of different habitats contrasts with the co‐occurring adaptive radiation of whitefish, which had a similar time span as roach to evolve in Lake Brienz, that is since the retreat of the glaciers ~12 kyrs ago. Within Lake Brienz, there are a total of four genetically differentiated whitefish species, segregated along the water depth and pelagic–benthic axes, which are distinct in their morphology, including the gill rakers (Doenz et al., ), thus suggesting adaptation to different trophic niches (Roesch, Lundsgaard‐Hansen, Vonlanthen, Taverna, & Seehausen, ). Given the abundances of perch and whitefish in Lake Brienz (Alexander et al., ; Doenz et al., ), the limited degree of diversification in roach could be a result of different factors: (a) Interspecific competition may have constrained roach from diversifying, (b) If the observed phenotypic differentiation (Figure ) is primarily due to phenotypic plasticity, the latter could have constrained diversification by shielding the genome from selection, thus decreasing the potential for genetic divergence (Ghalambor et al., ; Price et al., ), (c) The fundamental niche of roach may be narrower than that of whitefish, preventing roach to explore otherwise available niche space.…”

“…Within Lake Brienz, there are a total of four genetically differentiated whitefish species, segregated along the water depth and pelagic–benthic axes, which are distinct in their morphology, including the gill rakers (Doenz et al., ), thus suggesting adaptation to different trophic niches (Roesch, Lundsgaard‐Hansen, Vonlanthen, Taverna, & Seehausen, ). Given the abundances of perch and whitefish in Lake Brienz (Alexander et al., ; Doenz et al., ), the limited degree of diversification in roach could be a result of different factors: (a) Interspecific competition may have constrained roach from diversifying, (b) If the observed phenotypic differentiation (Figure ) is primarily due to phenotypic plasticity, the latter could have constrained diversification by shielding the genome from selection, thus decreasing the potential for genetic divergence (Ghalambor et al., ; Price et al., ), (c) The fundamental niche of roach may be narrower than that of whitefish, preventing roach to explore otherwise available niche space. For example, roach prefer warmer water and are therefore restricted to the shallow zones of lakes, whereas whitefish can tolerate colder water, allowing them to explore the deeper sections of lakes (Coutant, ; Kottelat & Freyhof, ), and (d) Recent genomic work suggests that adaptive diversification in stickleback and whitefish often occurs from standing genetic variation in genomic regions that show structural changes, including inversions (Jones et al., ; Marques et al., ) or chromosomal rearrangements (Dion‐Côté et al., ).…”

“…The slight differentiation of roach of different habitats contrasts with the co-occurring adaptive radiation of whitefish, which had a similar time span as roach to evolve in Lake Brienz, that is since the retreat of the glaciers ~12 kyrs ago. Within Lake Brienz, there are a total of four genetically differentiated whitefish species, segregated along the water depth and pelagic-benthic axes, which are distinct in their morphology, including the gill rakers (Doenz et al, 2018), thus suggesting adaptation to different trophic niches (Roesch, Lundsgaard-Hansen, Vonlanthen, Taverna, & Seehausen, 2013). Given the abundances of perch and whitefish in Lake Brienz (Alexander et al, 2015a;Doenz et al, 2018), the limited degree of diversification in roach could be a result of different factors: (a)…”

Case studies and mathematical models of ecological speciation. V. Adaptive divergence of whitefish in Fennoscandia

“…Baikal Cottus and various members of Salvelinus, in very large lakes using species-specific parameters. [71][72][73] Recent empirical studies have highlighted the important role of deep water habitats454 which have been previously neglected in monitoring efforts.74,75 In these respects, mathematical modeling could provide an efficient predictive tool for finding new lakes with three morphs, as well456 as identification of key factors contributing to their disappearance from the postglacial lakes.…”