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

Intraspecific differentiation in response to divergent natural selection between environments is a common phenomenon in some northern freshwater fishes, especially salmonids and stickleback. Understanding why these taxa diversify and undergo adaptive radiations while most other fish species in the same environments do not, remains an open question. The possibility for intraspecific diversification has rarely been evaluated for most northern freshwater fish species. Here, we assess the potential for intraspecific differentiation between and within lake populations of roach (Rutilus rutilus)-a widespread and abundant cyprinid species-in lakes in which salmonids have evolved endemic adaptive radiations. Based on more than 3,000 polymorphic RADseq markers, we detected low but significant genetic differentiation between roach populations of two ultraoligotrophic lakes and between these and populations from other lakes. This, together with differentiation in head morphology and stable isotope signatures, suggests evolutionary and ecological differentiation among some of our studied populations. Next, we tested for intralacustrine diversification of roach within Lake Brienz, the most pristine lake surveyed in this study. We found significant phenotypic evidence for ecological intralacustrine differentiation between roach caught over a muddy substrate and those caught over a rocky substrate. However, evidence for intralacustrine genetic differentiation is at best subtle and phenotypic changes may therefore be mostly plastic. Overall, our findings suggest roach can differ between ecologically distinct lakes, but the extent of intralacustrine ecological differentiation is weak, which contrasts with the strong differentiation among endemic species of whitefish in the same lakes.

Genomic signatures of relaxed disruptive selection associated with speciation reversal in whitefish.

BACKGROUND: Speciation reversal: the erosion of species differentiation via an increase in introgressive hybridization due to the weakening of previously divergent selection regimes, is thought to be an important, yet poorly understood, driver of biodiversity loss. Our study system, the Alpine whitefish (Coregonus spp.) species complex is a classic example of a recent postglacial adaptive radiation: forming an array of endemic lake flocks, with the independent origination of similar ecotypes among flocks. However, many of the lakes of the Alpine radiation have been seriously impacted by anthropogenic nutrient enrichment, resulting in a collapse in neutral genetic and phenotypic differentiation within the most polluted lakes. Here we investigate the effects of eutrophication on the selective forces that have shaped this radiation, using population genomics. We studied eight sympatric species assemblages belonging to five independent parallel adaptive radiations, and one species pair in secondary contact. We used AFLP markers, and applied FST outlier (BayeScan, Dfdist) and logistic regression analyses (MatSAM), to identify candidate regions for disruptive selection in the genome and their associations with adaptive traits within each lake flock. The number of outlier and adaptive trait associated loci identified per lake were then regressed against two variables (historical phosphorus concentration and contemporary oxygen concentration) representing the strength of eutrophication. RESULTS: Whilst we identify disruptive selection candidate regions in all lake flocks, we find similar trends, across analysis methods, towards fewer disruptive selection candidate regions and fewer adaptive trait/candidate loci associations in the more polluted lakes. CONCLUSIONS: Weakened disruptive selection and a concomitant breakdown in reproductive isolating mechanisms in more polluted lakes has lead to increased gene flow between coexisting Alpine whitefish species. We hypothesize that the resulting higher rates of interspecific recombination reduce either the number or extent of genomic islands of divergence surrounding loci evolving under disruptive natural selection. This produces the negative trend seen in the number of selection candidate loci recovered during genome scans of whitefish species flocks, with increasing levels of anthropogenic eutrophication: as the likelihood decreases that AFLP restriction sites will fall within regions of heightened genomic divergence and therefore be classified as F(ST) outlier loci. This study explores for the first time the potential effects of human-mediated relaxation of disruptive selection on heterogeneous genomic divergence between coexisting species.

Rapid parallel adaptive radiations from a single hybridogenic ancestral population.

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.

A taxonomic revision of the whitefish of lakes Brienz and Thun, Switzerland, with descriptions of four new species (Teleostei, Coregonidae).

The alpha taxonomy of the endemic whitefish of lakes Brienz and Thun, Switzerland, is revised. We evaluate the status of seven known species: Coregonus steinmanni sp. nov., Coregonus profundus sp. nov. and Coregonus acrinasus sp. nov. are endemic to Lake Thun; Coregonus Brienzii sp. nov. is endemic to Lake Brienz; and C. alpinus, C. albellus, and C. fatioi from lakes Brienz and Thun are redescribed. One of these species, C. alpinus, is revised, since the lectotype for this species is incongruent with the species description given by Kottelat (1997) and Kottelat and Freyhof (2007). The name C. alpinus is thus retained for the lectotype designated by Kottelat (1997) and a new description of this taxon provided. For the species otherwise described by Kottelat (1997) and Kottelat and Freyhof (2007) as C. alpinus the new name C. profundus is designated. Coregonus acrinasus is genetically partially of allochthonous origin, closely related to the radiation of Lake Constance, and we therefore compare it to all recognized species of Lake Constance, C. wartmanni, C. macrophthalmus, C. arenicolus, and C. gutturosus.

Colonization history of the Swiss Rhine basin by the bullhead (Cottus gobio): inference under a Bayesian spatially explicit framework.

The present distribution of freshwater fish in the Alpine region has been strongly affected by colonization events occurring after the last glacial maximum (LGM), some 20,000 years ago. We use here a spatially explicit simulation framework to model and better understand their colonization dynamics in the Swiss Rhine basin. This approach is applied to the European bullhead (Cottus gobio), which is an ideal model organism to study fish past demographic processes since it has not been managed by humans. The molecular diversity of eight sampled populations is simulated and compared to observed data at six microsatellite loci under an approximate Bayesian computation framework to estimate the parameters of the colonization process. Our demographic estimates fit well with current knowledge about the biology of this species, but they suggest that the Swiss Rhine basin was colonized very recently, after the Younger Dryas some 6600 years ago. We discuss the implication of this result, as well as the strengths and limits of the spatially explicit approach coupled to the approximate Bayesian computation framework.

Rapid buildup of sympatric species diversity in Alpine whitefish.

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.

Does eutrophication-driven evolution change aquatic ecosystems?

Eutrophication increases primary production and changes the relative abundance, taxonomic composition and spatial distribution of primary producers within an aquatic ecosystem. The changes in composition and location of resources alter the distribution and flow of energy and biomass throughout the food web. Changes in productivity also alter the physico-chemical environment, which has further effects on the biota. Such ecological changes influence the direction and strength of natural and sexual selection experienced by populations. Besides altering selection, they can also erode the habitat gradients and/or behavioural mechanisms that maintain ecological separation and reproductive isolation among species. Consequently, eutrophication of lakes commonly results in reduced ecological specialization as well as genetic and phenotypic homogenization among lakes and among niches within lakes. We argue that the associated loss in functional diversity and niche differentiation may lead to decreased carrying capacity and lower resource-use efficiency by consumers. We show that in central European whitefish species radiations, the functional diversity affected by eutrophication-induced speciation reversal correlates with community-wide trophic transfer efficiency (fisheries yield per unit phosphorus). We take this as an example of how evolutionary dynamics driven by anthropogenic environmental change can have lasting effects on biodiversity and ecosystem functioning.This article is part of the themed issue 'Human influences on evolution, and the ecological and societal consequences'.

Managing cryptic biodiversity: Fine-scale intralacustrine speciation along a benthic gradient in Alpine whitefish (Coregonus spp.).

Whitefish (Coregonus spp.) are an important catch for many freshwater fisheries, particularly in Switzerland. In support of this, supplemental stocking of whitefish species is carried out, despite lacking complete knowledge of the extent, distribution and origin of whitefish diversity in these lakes, potentially threatening local endemics via artificial gene flow. Here, we investigate phenotypic and genetic differentiation among coexisting whitefish species spawning along a depth gradient in a subalpine Swiss lake to better delineate intralacustrine whitefish biodiversity. We find depth-related clines in adaptive morphology and in neutral genetic markers. This individual variation is structured in three distinct clusters with spatial overlap. Individual genetic distances correlate strongly with differences in growth rate and gill-raker number, consistent with predictions of isolation-by-adaptation and ecological speciation. Genetic differentiation between species suggests reproductive isolation, despite demographic admixture on spawning grounds. Our results are consistent with clinal speciation resulting in three species coexisting in close ecological parapatry, one (C. sp. "benthic intermediate") being previously unknown. A second unknown species spawning in close proximity was found to be of potential allochthonous origin. This study highlights the importance of taxonomically unbiased sampling strategies to both understand evolutionary mechanisms structuring biodiversity and to better inform conservation and fisheries management.