Genomic insights into the vulnerability of sympatric whitefish species flocks

The erosion of habitat heterogeneity can reduce species diversity directly but can also lead to the loss of distinctiveness of sympatric species through speciation reversal. We know little about changes in genomic differentiation during the early stages of these processes, which can be mediated by anthropogenic perturbation. Here, we analyse three sympatric whitefish species (Coregonus spp) sampled across two neighbouring and connected Swiss pre‐alpine lakes, which have been differentially affected by anthropogenic eutrophication. Our data set comprises 16,173 loci genotyped across 138 whitefish using restriction‐site associated DNA sequencing (RADseq). Our analysis suggests that in each of the two lakes the population of a different, but ecologically similar, whitefish species declined following a recent period of eutrophication. Genomic signatures consistent with hybridisation are more pronounced in the more severely impacted lake. Comparisons between sympatric pairs of whitefish species with contrasting ecology, where one is shallow benthic and the other one more profundal pelagic, reveal genomic differentiation that is largely correlated along the genome, while differentiation is uncorrelated between pairs of allopatric provenance with similar ecology. We identify four genomic loci that provide evidence of parallel divergent adaptation between the shallow benthic species and the two different more profundal species. Functional annotations available for two of those loci are consistent with divergent ecological adaptation. Our genomic analysis indicates the action of divergent natural selection between sympatric whitefish species in pre‐alpine lakes and reveals the vulnerability of these species to anthropogenic alterations of the environment and associated adaptive landscape

Genetic architecture of adaptive radiation across two trophic levels

Evolution of trophic diversity is a hallmark of adaptive radiation. Yet, transitions between carnivory and herbivory are rare in young adaptive radiations. Haplochromine cichlid fish of the African Great Lakes are exceptional in this regard. Lake Victoria was colonized by an insectivorous generalist and in less than 20 000 years, several clades of specialized herbivores evolved. Carnivorous versus herbivorous lifestyles in cichlids require many different adaptations in functional morphology, physiology and behaviour. Ecological transitions in either direction thus require many traits to change in a concerted fashion, which could be facilitated if genomic regions underlying these traits were physically linked or pleiotropic. However, linkage/pleiotropy could also constrain evolvability. To investigate components of the genetic architecture of a suite of traits that distinguish invertivores from algae scrapers, we performed quantitative trait locus (QTL) mapping using a second-generation hybrid cross. While we found indications of linkage/pleiotropy within trait complexes, QTLs for distinct traits were distributed across several unlinked genomic regions. Thus, a mixture of independently segregating variation and some pleiotropy may underpin the rapid trophic transitions. We argue that the emergence and maintenance of associations between the different genomic regions underpinning co-adapted traits that evolved and persist against some gene flow required reproductive isolation

Rediscovery of a presumed extinct species, Salvelinus profundus, after re-oligotrophication

Lake Constance (47° 38’ N, 9° 22’ E) is a deep (max. depth 251m) and large (surface area 536 km2) postglacial lake in Central Europe. Originally, it harboured two charr species – Salvelinus umbla and S. profundus. The first is a medium-sized, colourful, winter spawning charr, which is widespread across Central European lakes, the second a small, pale, summer spawning, deepwater charr, which is endemic to Lake Constance (Schillinger 1901, Kottelat and Freyhof 2007). S. profundus has exceptionally large eyes and the upper jaw strongly overlaps the lower jaw. These traits are both considered adaptations to its life in the deep where it mostly feeds on profundal benthos (Schillinger 1901). During the second half of the last century, Lake Constance became eutrophic, resulting in oxygen-depletion in deep waters (IGKB 2004). The anoxic conditions harmed the development of eggs by profundal spawning fish (Baer et al. 2017). Thanks to strict management interventions, the lake has returned to an oligotrophic state, and oxygen is again available in the water column down to the greatest depth (IGKB 2004)

A taxonomic revision of ten whitefish species from the lakes Lucerne, Sarnen, Sempach and Zug, Switzerland, with descriptions of seven new species (Teleostei, Coregonidae)

The taxonomy of the endemic whitefish of the lakes of the Reuss River system (Lucerne, Sarnen, Zug) and Lake Sempach, Switzerland, is reviewed and revised. Lake Lucerne harbours five species. Coregonus intermundia sp. nov. and C. suspensus sp. nov., are described. Coregonus nobilis Haack, 1882, C. suidteri Fatio, 1885, and C. zugensis Nüsslin, 1882, are redescribed. Genetic studies have shown that C. suidteri and C. zugensis are composed of several distinct species endemic to different lakes. The names C. suidteri and C. zugensis are restricted to the species of lakes Sempach and Zug, respectively. The whitefish populations previously referred to as C. suidteri and C. zugensis from Lake Lucerne are described as C. litoralis sp. nov. and C. muelleri sp. nov., respectively. Furthermore, the whitefish from Lake Zug that were previously referred to as C. suidteri are described as C. supersum sp. nov. A holotype is designated for C. supersum that was previously one of two syntypes of C. zugensis. The other syntype is retained for C. zugensis. Coregonus obliterus sp. nov. is described from Lake Zug, and C. obliterus and C. zugensis from Lake Zug are extinct. Finally, we describe C. sarnensis sp. nov. from lakes Sarnen and Alpnach. Coregonus suidteri from Lake Sempach shows strong signals of introgression from deliberately translocated non-native whitefish species, which questions if the extant population still carries a genetic legacy from the original species and thus may need to be considered extinct. Coregonus suspensus is genetically partially of allochthonous origin, closely related to the radiation of Lake Constance. It is therefore compared to all known and described species of Lake Constance: C. wartmanni Bloch, 1784, C. macrophthalmus Nüsslin, 1882, C. arenicolus Kottelat,1997, and C. gutturosus Gmelin, 1818

Competition among small individuals hinders adaptive radiation despite ecological opportunity.

Ontogenetic diet shifts, where individuals change their resource use during development, are the rule rather than the exception in the animal world. Here, we aim to understand how such changes in diet during development affect the conditions for an adaptive radiation in the presence of ecological opportunity. We use a size-structured consumer-resource model and the adaptive dynamics approach to study the ecological conditions for speciation. We assume that small individuals all feed on a shared resource. Large individuals, on the other hand, have access to multiple food sources on which they can specialize. We find that competition among small individuals can hinder an adaptive radiation to unfold, despite plenty of ecological opportunity for large individuals. When small individuals experience strong competition for food, they grow slowly and only a few individuals are recruited to the larger size classes. Hence, competition for food among large individuals is weak and there is therefore no disruptive selection. In addition, initial conditions determine if an adaptive radiation occurs or not. A consumer population initially dominated by small individuals will not radiate. On the other hand, a population initially dominated by large individuals may undergo adaptive radiation and diversify into multiple species

Transgressive segregation in mating traits drives hybrid speciation.

Hybridization can rapidly generate novel genetic variation, which can promote ecological speciation by creating novel adaptive phenotypes. However, it remains unclear how hybridization, creating novel mating phenotypes (e.g., mating season, genitalia shapes, sexual displays, mate preferences), affects speciation especially when the phenotypes do not confer adaptive advantages. Here, based on individual-based evolutionary simulations, we propose that transgressive segregation of mating traits can drive incipient hybrid speciation. Simulations demonstrated that incipient hybrid speciation occurred most frequently when the hybrid population received moderate continued immigration from parental lineages causing recurrent episodes of hybridization. Recurrent hybridization constantly generated genetic variation, which promoted the rapid stochastic evolution of mating phenotypes in a hybrid population. The stochastic evolution continued until a novel mating phenotype came to dominate the hybrid population, which reproductively isolates the hybrid population from parental lineages. However, too frequent hybridization rather hindered the evolution of reproductive isolation by inflating the variation of mating phenotypes to produce phenotypes allowing mating with parental lineages. Simulations also revealed conditions for long-term persistence of hybrid species after their incipient emergence. Our results suggest that recurrent transgressive segregation of mating phenotypes can offer a plausible explanation for hybrid speciation and radiations that involved little adaptive ecological divergence

Morphological Diversity and the Roles of Contingency, Chance and Determinism in African Cichlid Radiations

BACKGROUND: Deterministic evolution, phylogenetic contingency and evolutionary chance each can influence patterns of morphological diversification during adaptive radiation. In comparative studies of replicate radiations, convergence in a common morphospace implicates determinism, whereas non-convergence suggests the importance of contingency or chance. METHODOLOGY/PRINCIPAL FINDINGS: The endemic cichlid fish assemblages of the three African great lakes have evolved similar sets of ecomorphs but show evidence of non-convergence when compared in a common morphospace, suggesting the importance of contingency and/or chance. We then analyzed the morphological diversity of each assemblage independently and compared their axes of diversification in the unconstrained global morphospace. We find that despite differences in phylogenetic composition, invasion history, and ecological setting, the three assemblages are diversifying along parallel axes through morphospace and have nearly identical variance-covariance structures among morphological elements. CONCLUSIONS/SIGNIFICANCE: By demonstrating that replicate adaptive radiations are diverging along parallel axes, we have shown that non-convergence in the common morphospace is associated with convergence in the global morphospace. Applying these complimentary analyses to future comparative studies will improve our understanding of the relationship between morphological convergence and non-convergence, and the roles of contingency, chance and determinism in driving morphological diversification

A Combinatorial View on Speciation and Adaptive Radiation.

Speciation is often thought of as a slow process due to the waiting times for mutations that cause incompatibilities, and permit ecological differentiation or assortative mating. Cases of rapid speciation and particularly cases of rapid adaptive radiation into multiple sympatric species have remained somewhat mysterious. We review recent findings from speciation genomics that reveal an emerging commonality among such cases: reassembly of old genetic variation into new combinations facilitating rapid speciation and adaptive radiation. The polymorphisms in old variants frequently originated from hybridization at some point in the past. We discuss why old variants are particularly good fuel for rapid speciation, and hypothesize that variation in access to such old variants might contribute to the large variation in speciation rates observed in nature