Diverse pathways to speciation revealed by marine snails.

Speciation is a key evolutionary process that is not yet fully understood. Combining population genomic and ecological data from multiple diverging pairs of marine snails (Littorina) supports the search for speciation mechanisms. Placing pairs on a one-dimensional speciation continuum, from undifferentiated populations to species, obscured the complexity of speciation. Adding multiple axes helped to describe either speciation routes or reproductive isolation in the snails. Divergent ecological selection repeatedly generated barriers between ecotypes, but appeared less important in completing speciation while genetic incompatibilities played a key role. Chromosomal inversions contributed to genomic barriers, but with variable impact. A multidimensional (hypercube) approach supported framing of questions and identification of knowledge gaps and can be useful to understand speciation in many other systems.

The Impact of Chromosomal Rearrangements in Speciation: From Micro- to Macroevolution.

Chromosomal rearrangements (CRs) have been known since almost the beginning of genetics. While an important role for CRs in speciation has been suggested, evidence primarily stems from theoretical and empirical studies focusing on the microevolutionary level (i.e., on taxon pairs where speciation is often incomplete). Although the role of CRs in eukaryotic speciation at a macroevolutionary level has been supported by associations between species diversity and rates of evolution of CRs across phylogenies, these findings are limited to a restricted range of CRs and taxa. Now that more broadly applicable and precise CR detection approaches have become available, we address the challenges in filling some of the conceptual and empirical gaps between micro- and macroevolutionary studies on the role of CRs in speciation. We synthesize what is known about the macroevolutionary impact of CRs and suggest new research avenues to overcome the pitfalls of previous studies to gain a more comprehensive understanding of the evolutionary significance of CRs in speciation across the tree of life.

Ten years of demographic modelling of divergence and speciation in the sea.

Understanding population divergence that eventually leads to speciation is essential for evolutionary biology. High species diversity in the sea was regarded as a paradox when strict allopatry was considered necessary for most speciation events because geographical barriers seemed largely absent in the sea, and many marine species have high dispersal capacities. Combining genome-wide data with demographic modelling to infer the demographic history of divergence has introduced new ways to address this classical issue. These models assume an ancestral population that splits into two subpopulations diverging according to different scenarios that allow tests for periods of gene flow. Models can also test for heterogeneities in population sizes and migration rates along the genome to account, respectively, for background selection and selection against introgressed ancestry. To investigate how barriers to gene flow arise in the sea, we compiled studies modelling the demographic history of divergence in marine organisms and extracted preferred demographic scenarios together with estimates of demographic parameters. These studies show that geographical barriers to gene flow do exist in the sea but that divergence can also occur without strict isolation. Heterogeneity of gene flow was detected in most population pairs suggesting the predominance of semipermeable barriers during divergence. We found a weak positive relationship between the fraction of the genome experiencing reduced gene flow and levels of genome-wide differentiation. Furthermore, we found that the upper bound of the 'grey zone of speciation' for our dataset extended beyond that found before, implying that gene flow between diverging taxa is possible at higher levels of divergence than previously thought. Finally, we list recommendations for further strengthening the use of demographic modelling in speciation research. These include a more balanced representation of taxa, more consistent and comprehensive modelling, clear reporting of results and simulation studies to rule out nonbiological explanations for general results.

Parthenogenesis in Darevskia lizards: A rare outcome of common hybridization, not a common outcome of rare hybridization.

Hybridization is a common evolutionary process with multiple possible outcomes. In vertebrates, interspecific hybridization has repeatedly generated parthenogenetic hybrid species. However, it is unknown whether the generation of parthenogenetic hybrids is a rare outcome of frequent hybridization between sexual species within a genus or the typical outcome of rare hybridization events. Darevskia is a genus of rock lizards with both hybrid parthenogenetic and sexual species. Using capture sequencing, we estimate phylogenetic relationships and gene flow among the sexual species, to determine how introgressive hybridization relates to the origins of parthenogenetic hybrids. We find evidence for widespread hybridization with gene flow, both between recently diverged species and deep branches. Surprisingly, we find no signal of gene flow between parental species of the parthenogenetic hybrids, suggesting that the parental pairs were either reproductively or geographically isolated early in their divergence. The generation of parthenogenetic hybrids in Darevskia is, then, a rare outcome of the total occurrence of hybridization within the genus, but the typical outcome when specific species pairs hybridize. Our results question the conventional view that parthenogenetic lineages are generated by hybridization in a window of divergence. Instead, they suggest that some lineages possess specific properties that underpin successful parthenogenetic reproduction.

Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers.

Speciation, that is, the evolution of reproductive barriers eventually leading to complete isolation, is a crucial process generating biodiversity. Recent work has contributed much to our understanding of how reproductive barriers begin to evolve, and how they are maintained in the face of gene flow. However, little is known about the transition from partial to strong reproductive isolation (RI) and the completion of speciation. We argue that the evolution of strong RI is likely to involve different processes, or new interactions among processes, compared with the evolution of the first reproductive barriers. Transition to strong RI may be brought about by changing external conditions, for example, following secondary contact. However, the increasing levels of RI themselves create opportunities for new barriers to evolve and, and interaction or coupling among barriers. These changing processes may depend on genomic architecture and leave detectable signals in the genome. We outline outstanding questions and suggest more theoretical and empirical work, considering both patterns and processes associated with strong RI, is needed to understand how speciation is completed. This article is part of the theme issue 'Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.

Diversity and distribution of freshwater amphipod species in Switzerland (Crustacea: Amphipoda).

Amphipods are key organisms in many freshwater systems and contribute substantially to the diversity and functioning of macroinvertebrate communities. Furthermore, they are commonly used as bioindicators and for ecotoxicological tests. For many areas, however, diversity and distribution of amphipods is inadequately known, which limits their use in ecological and ecotoxicological studies and handicaps conservation initiatives. We studied the diversity and distribution of amphipods in Switzerland (Central Europe), covering four major drainage basins, an altitudinal gradient of>2,500 m, and various habitats (rivers, streams, lakes and groundwater). We provide the first provisional checklist and detailed information on the distribution and diversity of all amphipod species from Switzerland. In total, we found 29 amphipod species. This includes 16 native and 13 non-native species, one of the latter (Orchestia cavimana) reported here for the first time for Switzerland. The diversity is compared to neighboring countries. We specifically discuss species of the genus Niphargus, which are often receiving less attention. We also found evidence of an even higher level of hidden diversity, and the potential occurrence of further cryptic species. This diversity reflects the biogeographic past of Switzerland, and suggests that amphipods are ideally suited to address questions on endemism and adaptive radiations, post-glaciation re-colonization and invasion dynamics as well as biodiversity-ecosystem functioning relationships in aquatic systems.

Hidden biodiversity in an ecologically important freshwater amphipod: differences in genetic structure between two cryptic species.

Cryptic species, i.e. species that are morphologically hard to distinguish, have been detected repeatedly in various taxa and ecosystems. In order to evaluate the importance of this finding, we have to know in how far cryptic species differ in various aspects of their biology. The amphipod Gammarus fossarum is a key invertebrate in freshwater streams and contains several cryptic species. We examined the population genetic structure, genetic diversity and demographic history of two of them (type A and type B) using microsatellite markers and asked whether they show significant differences. We present results of population genetic analyses based on a total of 37 populations from the headwaters of two major European drainages, Rhine and Rhone. We found that, in both species, genetic diversity was geographically structured among and within drainages. For type A in the Rhine and type B in the Rhone, we detected significant patterns of isolation by distance. The increase of genetic differentiation with geographical distance, however, was much higher in type A than in type B. This result indicates substantial interspecific differences in population history and/or the extent of current gene flow between populations. In the Rhine, type B does not show evidence of isolation by distance, and population differentiation is relatively low across hundreds of kilometres. The majority of these populations also show signatures of recent bottlenecks. These patterns are consistent with a recent expansion of type B into the Rhine drainage. In summary, our results suggest considerable and previously unrecognized interspecific differences in the genetic structure of these cryptic keystone species.

Spatial distribution of cryptic species diversity in european freshwater amphipods (Gammarus fossarum) as revealed by pyrosequencing.

In order to understand and protect ecosystems, local gene pools need to be evaluated with respect to their uniqueness. Cryptic species present a challenge in this context because their presence, if unrecognized, may lead to serious misjudgement of the distribution of evolutionarily distinct genetic entities. In this study, we describe the current geographical distribution of cryptic species of the ecologically important stream amphipod Gammarus fossarum (types A, B and C). We use a novel pyrosequencing assay for molecular species identification and survey 62 populations in Switzerland, plus several populations in Germany and eastern France. In addition, we compile data from previous publications (mainly Germany). A clear transition is observed from type A in the east (Danube and Po drainages) to types B and, more rarely, C in the west (Meuse, Rhone, and four smaller French river systems). Within the Rhine drainage, the cryptic species meet in a contact zone which spans the entire G. fossarum distribution range from north to south. This large-scale geographical sorting indicates that types A and B persisted in separate refugia during Pleistocene glaciations. Within the contact zone, the species rarely co-occur at the same site, suggesting that ecological processes may preclude long-term coexistence. The clear phylogeographical signal observed in this study implies that, in many parts of Europe, only one of the cryptic species is present.