Denis Roy

Speciation reversal and biodiversity dynamics with hybridization in changing environments

A considerable fraction of the worlds biodiversity is of recent evolutionary origin and has evolved as a by‐product of, and is maintained by, divergent adaptation in heterogeneous environments. Conservationists have paid attention to genetic homogenization caused by human‐induced translocations (e.g. biological invasions and stocking), and to the importance of environmental heterogeneity for the ecological coexistence of species. However, far less attention has been paid to the consequences of loss of environmental heterogeneity to the genetic coexistence of sympatric species. Our review of empirical observations and our theoretical considerations on the causes and consequences of interspecific hybridization suggest that a loss of environmental heterogeneity causes a loss of biodiversity through increased genetic admixture, effectively reversing speciation. Loss of heterogeneity relaxes divergent selection and removes ecological barriers to gene flow between divergently adapted species, promoting interspecific introgressive hybridization. Since heterogeneity of natural environments is rapidly deteriorating in most biomes, the evolutionary ecology of speciation reversal ought to be fully integrated into conservation biology.

Eutrophication causes speciation reversal in whitefish adaptive radiations

Species diversity can be lost through two different but potentially interacting extinction processes: demographic decline and speciation reversal through introgressive hybridization. To investigate the relative contribution of these processes, we analysed historical and contemporary data of replicate whitefish radiations from 17 pre-alpine European lakes and reconstructed changes in genetic species differentiation through time using historical samples. Here we provide evidence that species diversity evolved in response to ecological opportunity, and that eutrophication, by diminishing this opportunity, has driven extinctions through speciation reversal and demographic decline. Across the radiations, the magnitude of eutrophication explains the pattern of species loss and levels of genetic and functional distinctiveness among remaining species. We argue that extinction by speciation reversal may be more widespread than currently appreciated. Preventing such extinctions will require that conservation efforts not only target existing species but identify and protect the ecological and evolutionary processes that generate and maintain species.

Hybridization between distant lineages increases adaptive variation during a biological invasion: stickleback in Switzerland

The three‐spined stickleback is a widespread Holarctic species complex that radiated from the sea into freshwaters after the retreat of the Pleistocene ice sheets. In Switzerland, sticklebacks were absent with the exception of the far northwest, but different introduced populations have expanded to occupy a wide range of habitats since the late 19th century. A well‐studied adaptive phenotypic trait in sticklebacks is the number of lateral plates. With few exceptions, freshwater and marine populations in Europe are fixed for either the low plated phenotype or the fully plated phenotype, respectively. Switzerland, in contrast, harbours in close proximity the full range of phenotypic variation known from across the continent. We addressed the phylogeographic origins of Swiss sticklebacks using mitochondrial partial cytochrome b and control region sequences. We found only five different haplotypes but these originated from three distinct European regions, fixed for different plate phenotypes. These lineages occur largely in isolation at opposite ends of Switzerland, but co‐occur in a large central part. Across the country, we found a strong correlation between a microsatellite linked to the high plate ectodysplasin allele and the mitochondrial haplotype from a region where the fully plated phenotype is fixed. Phylogenomic and population genomic analysis of 481 polymorphic amplified fragment length polymorphism loci indicate genetic admixture in the central part of the country. The same part of the country also carries elevated within‐population phenotypic variation. We conclude that during the recent invasive range expansion of sticklebacks in Switzerland, adaptive and neutral between‐population genetic variation was converted into within‐population variation, raising the possibility that hybridization between colonizing lineages contributed to the ecological success of sticklebacks in Switzerland.

Divergence along a steep ecological gradient in lake whitefish (Coregonus sp.)

To understand mechanisms structuring diversity in young adaptive radiations, quantitative and unbiased information about genetic and phenotypic diversity is much needed. Here, we present the first in‐depth investigation of whitefish diversity in a Swiss lake, with continuous spawning habitat sampling in both time and space. Our results show a clear cline like pattern in genetics and morphology of populations sampled along an ecological depth gradient in Lake Neuchâtel. Divergent natural selection appears to be involved in shaping this cline given that trait specific PST‐values are significantly higher than FST‐values when comparing populations caught at different depths. These differences also tend to increase with increasing differences in depth, indicating adaptive divergence along a depth gradient, which persists despite considerable gene flow between adjacent demes. It however remains unclear, whether the observed pattern is a result of currently stable selection‐gene flow balance, incipient speciation, or reverse speciation due to anthropogenic habitat alteration causing two formerly divergent species to collapse into a single gene pool.

Resource‐based adaptive divergence in the freshwater fish Telmatherina from Lake Matano, Indonesia

Adaptive radiations are an important source of biodiversity, but resolving which ecological pressures seed these processes in natural systems remains difficult. Here the adaptive radiation among Telmatherina, a genus of freshwater fish endemic to an ancient lake in central Sulawesi, Indonesia, was examined to determine its causal root. We demonstrate that all Telmatherina in this lake can be categorized into three lineages each possessing specialized skull shapes and pharyngeal jaw bones allowing them to exploit different resources. These data demonstrate a natural example of how resource partitioning has likely initiated adaptive radiation in a resource limited environment.

Genetic and morphological data supporting the hypothesis of adaptive radiation in the endemic fish of Lake Matano

Adaptive radiation resulting from differential selection acting on functional features is believed to be an important source of biodiversity. In this study, morphometric measures and mitochondrial DNA are used to test for adaptive radiation within four fish genera (Glossogobius, Oryzias, Dermogenys and Telmatherina) endemic to an ancient island lake (Lake Matano, Sulawesi, Indonesia), using the framework proposed by Schluter (The Ecology of Adaptive Radiation, Oxford University Press, 2000). We demonstrate common ancestry and rapid divergence in one genus (Telmatherina) based on 560 bp of 16S sequence data. We found higher levels of variation in feeding‐related traits (N = 8) for Telmatherina relative to the other genera, while no differences were found for sexual display traits (N = 8) or neutral morphological traits (N = 8). Telmatherina also had the highest number of distinct colouration patterns among the four genera. These data, combined with the very low productivity of the lake, are indicative of selection driving adaptive radiation. The morphometric divergence in the Telmatherina likely results from selection acting on feeding traits in this low productivity lake, leading to trophic specialization among closely related morphotypes. These results provide indirect but compelling data supporting the adaptive radiation of Telmatherina in this system.

Body shape vs. colour associated initial divergence in the Telmatherina radiation in Lake Matano, Sulawesi, Indonesia.

Highly polymorphic colouration patterns are often associated with sexual selection in fish and can be the initial cause of divergence among closely related taxa. Here we use genetic, body colour and geometric morphometric data collected on 118 fish from Lake Matano, Sulawesi, Indonesia to test if colouration is the initial cause of divergence in the radiating Telmatherina genus. Results reveal that all Telmatherina previously described in this system can be categorized into three mitochondrial lineages and that colouration is only weakly associated with early divergence. Clade‐specific body shapes, however, likely adapted to microenvironments are key to the initial divergence in this system. Data also show that although colourations were not likely instrumental in seeding divergence in these fish, they appear to have developed in parallel within each clade. Our results are consistent with an emerging pattern repeated in many vertebrate radiations, whereby divergence by colouration or other display traits is preceded by specialization to environmental adaptive peaks.

Hybrid ‘superswarm’ leads to rapid divergence and establishment of populations during a biological invasion

Understanding the genetic background of invading species can be crucial information clarifying why they become invasive. Intraspecific genetic admixture among lineages separated in the native ranges may promote the rate and extent of an invasion by substantially increasing standing genetic variation. Here, we examined the genetic relationships among threespine stickleback that recently colonized Switzerland. This invasion results from several distinct genetic lineages that colonized multiple locations and have since undergone range expansions, where they coexist and admix in parts of their range. Using 17 microsatellites genotyped for 634 individuals collected from 17 Swiss and two non‐Swiss European sites, we reconstruct the invasion of stickleback and investigate the potential and extent of admixture and hybridization among the colonizing lineages from a population genetic perspective. Specifically, we test for an increase in standing genetic variation in populations where multiple lineages coexist. We find strong evidence of massive hybridization early on, followed by what appears to be recent increased genetic isolation and the formation of several new genetically distinguishable populations, consistent with a hybrid ‘superswarm’. This massive hybridization and population formation event(s) occurred over approximately 140 years and likely fuelled the successful invasion of a diverse range of habitats. The implications are that multiple colonizations coupled with hybridization can lead to the formation of new stable genetic populations potentially kick‐starting speciation and adaptive radiation over a very short timescale.

Sexual dimorphism dominates divergent host plant use in stick insect trophic morphology.

BackgroundClear examples of ecological speciation exist, often involving divergence in trophic morphology. However, substantial variation also exists in how far the ecological speciation process proceeds, potentially linked to the number of ecological axes, traits, or genes subject to divergent selection. In addition, recent studies highlight how differentiation might occur between the sexes, rather than between populations. We examine variation in trophic morphology in two host-plant ecotypes of walking-stick insects (Timema cristinae), known to have diverged in morphological traits related to crypsis and predator avoidance, and to have reached an intermediate point in the ecological speciation process. Here we test how host plant use, sex, and rearing environment affect variation in trophic morphology in this species using traditional multivariate, novel kernel density based and Bayesian morphometric analyses.ResultsContrary to expectations, we find limited host-associated divergence in mandible shape. Instead, the main predictor of shape variation is sex, with secondary roles of population of origin and rearing environment.ConclusionOur results show that trophic morphology does not strongly contribute to host-adapted ecotype divergence in T. cristinae and that traits can respond to complex selection regimes by diverging along different intraspecific lines, thereby impeding progress toward speciation.

Correlating Shape Variation with Feeding Performance to Test for Adaptive Divergence in Recently Invading Stickleback Populations from Swiss peri-alpine Environments

The purpose of this chapter is to demonstrate the application of geometric morphometrics in a typical study, and put the information it provides into a broader context. Here we use geometric morphometrics to describe the head shape among three different Swiss stickleback populations from two drainages, including both lake and stream residents. Head shapes are compared to feeding efficiency indices generated from laboratory trials using lake and stream prey types. We also combine these data with genetic and other more traditional morphological assessments to understand the roots of the tremendous variation exhibited by sticklebacks in Switzerland. This work shows that in combination with other data, geometric morphometrics can make a significant contribution toward understanding the natural history of taxa and is an indispensible tool providing insight into fundamental mechanisms of adaptive divergence and speciation.