Ecological speciation in postglacialEuropean whitefish: rapid adaptive radiations into the littoral, pelagic, and profundal lake habitats

Abstract

Understanding how a monophyletic lineage of a species diverges into several adaptive forms has received increased attention in recent years, but the underlying mechanisms in this process are still under debate. Postglacial fishes are excellent model organisms for exploring this process, especially the initial stages of ecological speciation, as postglacial lakes represent replicated discrete environments with variation in available niches. Here, we combine data of niche utilization, trophic morphology, and 17 microsatellite loci to investigate the diversification process of three sympatric European whitefish morphs from three northern Fennoscandian lakes. The morphological divergence in the gill raker number among the whitefish morphs was related to the utilization of different trophic niches and was associated with reproductive isolation within and across lakes. The intralacustrine comparison of whitefish morphs showed that these systems represent two levels of adaptive divergence: (1) a consistent littoral–pelagic resource axis; and (2) a more variable littoral–profundal resource axis. The results also indicate that the profundal whitefish morph has diverged repeatedly from the ancestral littoral whitefish morph in sympatry in two different watercourses. In contrast, all the analyses performed revealed clustering of the pelagic whitefish morphs across lakes suggesting parallel postglacial immigration with the littoral whitefish morph into each lake. Finally, the analyses strongly suggested that the trophic adaptive trait, number of gill rakers, was under diversifying selection in the different whitefish morphs. Together, the results support a complex evolutionary scenario where ecological speciation acts, but where both allopatric (colonization history) and sympatric (within watercourse divergence) processes are involved.

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

“…“pelagic intermediate” (“ Pelagic intermediate ”). For the species found spawning along the depth gradient, we find a strong association of individual genetic variation with growth rate and gill‐raker counts, traits suggested to be evolving under divergent selection in whitefish (Østbye et al., 2006; Præbel et al., 2013; Rogers & Bernatchez, 2007; Vonlanthen et al., 2009). These findings are consistent with predictions of isolation‐by‐adaptation and ecological speciation along clines in our studied depth gradient (Funk, Nosil, & Etges, 2006; Nosil, 2012; Rundle & Nosil, 2005).…”

“…Alpine whitefish with lower gill‐raker densities, on the other hand, have been shown to be more efficient at foraging for large benthic prey items (Lundsgaard‐Hansen, Matthews, Vonlanthen, Taverna, & Seehausen, 2013). These predictable differences in feeding efficiency are suggestive of fitness trade‐offs in gill‐raker number between the respective niches of coexisting Alpine whitefish species, corroborated by genetic evidence that within‐lake patterns of gill‐raker count variation are driven by divergent natural selection regimes in the Alpine and other whitefish radiations (Hudson et al., 2013; Præbel et al., 2013; Rogers & Bernatchez, 2007; Vonlanthen et al., 2009). Whitefish growth rate is a complex physiological trait impinging on many other aspects of the overall phenotype such as body shape.…”

Evolution and origin of sympatric shallow-water morphotypes of Lake Trout, Salvelinus namaycush, in Canada’s Great Bear Lake

“…Specifically, our work supports the idea that post-glacial populations of fishes may diverge into discrete ecomorphological forms in sympatry subsequent to colonization of novel, heterogonous post-glacial habitats. Although empirical examples of divergence occurring sympatrically are still relatively rare (Bolnick and Fitzpatrick, 2007), more studies supporting this scenario are becoming available (for example, Barluenga et al, 2006), including an increasing number involving north temperate fishes (Taylor and Bentzen, 1993;Gíslason et al, 1999;Lu et al, 2001;Alekseyev et al, 2002;Praebel et al, 2013).…”

“…In many cases, there are also examples of repeated occurrences of divergent ecotypes within a taxon that appear to have evolved in parallel (Schluter and Nagel, 1995;Pigeon et al, 1997;Østbye et al, 2006), and there is evidence both for evolution of ecotypes in allopatry followed by secondary contact (Bernatchez and Dodson, 1990;Fraser and Bernatchez, 2005) and for sympatric divergence (Taylor and Bentzen, 1993;Praebel et al, 2013). Phenotypic plasticity, the capability of a genotype to exhibit variable phenotypes as influenced by the environment (Whitman and Agrawal, 2009) has also been important in generating morphological and ecological diversity in post-glacial habitats (Robinson and Parsons, 2002).…”

Allometric trajectories of body and head morphology in three sympatric Arctic charr (Salvelinus alpinus (L.)) morphs

“…Diversification and speciation often follow colonization of new environments (Orr & Smith, 1998; Price, Qvarnström, & Irwin, 2003) and an intermediate step toward speciation is often the evolution of morphs that utilize different resources, such as habitat and food (Pfennig et al., 2010; Smith & Skúlason, 1996). Thus, resource polymorphism is a recognized step in ecological speciation, especially when it occurs in sympatry (Berlocher & Feder, 2002; Schliewen, Tautz, & Pääbo, 1994; Via, 2001) and may eventually lead to reproductive isolated populations of eco‐morphs (Præbel et al., 2013; Rundle & Nosil, 2005; Wimberger, 1994). Factors that may promote resource polymorphism are vacant niches, habitat variability, and relaxation of interspecific competition (Smith & Skúlason, 1996).…”