Fabrice Eroukhmanoff

Hybridization and speciation

Hybridization has many and varied impacts on the process of speciation. Hybridization may slow or reverse differentiation by allowing gene flow and recombination. It may accelerate speciation via adaptive introgression or cause near‐instantaneous speciation by allopolyploidization. It may have multiple effects at different stages and in different spatial contexts within a single speciation event. We offer a perspective on the context and evolutionary significance of hybridization during speciation, highlighting issues of current interest and debate. In secondary contact zones, it is uncertain if barriers to gene flow will be strengthened or broken down due to recombination and gene flow. Theory and empirical evidence suggest the latter is more likely, except within and around strongly selected genomic regions. Hybridization may contribute to speciation through the formation of new hybrid taxa, whereas introgression of a few loci may promote adaptive divergence and so facilitate speciation. Gene regulatory networks, epigenetic effects and the evolution of selfish genetic material in the genome suggest that the Dobzhansky–Muller model of hybrid incompatibilities requires a broader interpretation. Finally, although the incidence of reinforcement remains uncertain, this and other interactions in areas of sympatry may have knock‐on effects on speciation both within and outside regions of hybridization.

Genomics and the origin of species

Speciation is a fundamental evolutionary process, the knowledge of which is crucial for understanding the origins of biodiversity. Genomic approaches are an increasingly important aspect of this research field. We review current understanding of genome-wide effects of accumulating reproductive isolation and of genomic properties that influence the process of speciation. Building on this work, we identify emergent trends and gaps in our understanding, propose new approaches to more fully integrate genomics into speciation research, translate speciation theory into hypotheses that are testable using genomic tools and provide an integrative definition of the field of speciation genomics.

Effects of natural and sexual selection on adaptive population divergence and premating isolation in a damselfly.

Abstract The relative strength of different types of directional selection has seldom been compared directly in natural populations. A recent meta-analysis of phenotypic selection studies in natural populations suggested that directional sexual selection may be stronger in magnitude than directional natural selection, although this pattern may have partly been confounded by the different time scales over which selection was estimated. Knowledge about the strength of different types of selection is of general interest for understanding how selective forces affect adaptive population divergence and how they may influence speciation. We studied divergent selection on morphology in parapatric, natural damselfly (Calopteryx splendens) populations. Sexual selection was stronger than natural selection measured on the same traits, irrespective of the time scale over which sexual selection was measured. Visualization of the fitness surfaces indicated that population divergence in overall morphology is more strongly influenced by divergent sexual selection rather than natural selection. Courtship success of experimental immigrant males was lower than that of resident males, indicating incipient sexual isolation between these populations. We conclude that current and strong sexual selection promotes adaptive population divergence in this species and that premating sexual isolation may have arisen as a correlated response to divergent sexual selection. Our results highlight the importance of sexual selection, rather than natural selection in the adaptive radiation of odonates, and supports previous suggestions that divergent sexual selection promotes speciation in this group.

Gender Differences in Species Recognition and the Evolution of Asymmetric Sexual Isolation

Closely related sympatric species are expected to evolve strong species discrimination because of the reinforcement of mate preferences. Fitness costs of heterospecific matings are thought to be higher in females than in males, and females are therefore expected to show stronger species discrimination than males. Here, we investigated gender and species differences in sexual isolation in a sympatric species pair of Calopteryx damselflies. The genus Calopteryx is one of the classic examples of reproductive character displacement in evolutionary biology, with exaggerated interspecific differences in the amount of dark wing coloration when species become sympatric. Experimental manipulation of the extent of dark wing coloration revealed that sexual isolation results from both female and male mate discrimination and that wing melanization functions as a species recognition character. Female choice of conspecific males is entirely based on wing coloration, whereas males in one species also use other species recognition cues in addition to wing color. Stronger species discrimination ability in males is presumably an evolutionary response to an elevated male predation risk caused by conspicuous wing coloration. Gender differences in species discrimination and fitness costs of male courtship can thus shed new light on the evolution of asymmetric sexual isolation and the reinforcement of mate preferences.

A ROLE FOR LEARNING IN POPULATION DIVERGENCE OF MATE PREFERENCES.

Learning and other forms of phenotypic plasticity have been suggested to enhance population divergence. Mate preferences can develop by learning, and species recognition might not be entirely genetic. We present data on female mate preferences of the banded demoiselle (Calopteryx splendens) that suggest a role for learning in population divergence and species recognition. Populations of this species are either allopatric or sympatric with a phenotypically similar congener (C. virgo). These two species differ mainly in the amount of wing melanization in males, and wing patches thus mediate sexual isolation. In sympatry, sexually experienced females discriminate against large melanin wing patches in heterospecific males. In contrast, in allopatric populations within the same geographic region, females show positive (“open‐ended”) preferences for such large wing patches. Virgin C. splendens females do not discriminate against heterospecific males. Moreover, physical exposure experiments of such virgin females to con‐ or hetero‐specific males significantly influences their subsequent mate preferences. Species recognition is thus not entirely genetic and it is partly influenced by interactions with mates. Learning causes pronounced population divergence in mate preferences between these weakly genetically differentiated populations, and results in a highly divergent pattern of species recognition at a small geographic scale.

Parallelism and historical contingency during rapid ecotype divergence in an isopod

Recent studies on parallel evolution have focused on the relative role of selection and historical contingency during adaptive divergence. Here, we study geographically separate and genetically independent lake populations of a freshwater isopod (Asellus aquaticus) in southern Sweden. In two of these lakes, a novel habitat was rapidly colonized by isopods from a source habitat. Rapid phenotypic changes in pigmentation, size and sexual behaviour have occurred, presumably in response to different predatory regimes. We partitioned the phenotypic variation arising from habitat (‘selection’: 81–94%), lake (‘history’: 0.1–6%) and lake × habitat interaction (‘unique diversification’: 0.4–13%) for several traits. There was a limited role for historical contingency but a strong signature of selection. We also found higher phenotypic variation in the source populations. Phenotype sorting during colonization and strong divergent selection might have contributed to these rapid changes. Consequently, phenotypic divergence was only weakly influenced by historical contingency.

Evolution and stability of the G-matrix during the colonization of a novel environment

Populations that undergo a process of rapid evolution present excellent opportunities to investigate the mechanisms driving or restraining adaptive divergence. The genetic variance–covariance matrix (G) is often considered to constrain adaptation but little is known about its potential to evolve during phenotypic divergence. We compared the G‐matrices of ancestral and recently established ecotype populations of an aquatic isopod (Asellus aquaticus) that have diverged in parallel in two south Swedish lakes. Phenotypic changes after colonization involved a reduction in overall size, lost pigmentation and changes in shape. Comparisons between G‐matrices reveal close similarity within the same ecotype from different lakes but some degree of differentiation among ecotypes. Phenotypic divergence has apparently not been much influenced by the orientation of G. Additive genetic variation in the newly colonized habitats has also decreased substantially. This suggests that a process of adaptation from standing genetic variation has occurred and has probably facilitated phenotypic divergence.

Contemporary Parallel Diversification, Antipredator Adaptations and Phenotypic Integration in an Aquatic Isopod

It is increasingly being recognized that predation can be a strong diversifying agent promoting ecological divergence. Adaptations against different predatory regimes can emerge over short periods of time and include many different traits. We studied antipredator adaptations in two ecotypes of an isopod (Asellus aquaticus) that have, diverged in parallel in two Swedish lakes over the last two decades. We quantified differences in escape speed, morphology and behavior for isopods from different ecotypes present in these lakes. Isopods from the source habitat (reed) coexist with mainly invertebrate predators. They are more stream-profiled and have higher escape speeds than isopods in the newly colonized stonewort habitat, which has higher density of fish predators. Stonewort isopods also show more cautious behaviors and had higher levels of phenotypic integration between coloration and morphological traits than the reed isopods. Colonization of a novel habitat with a different predation regime has thus strengthened the correlations between pigmentation and morphology and weakened escape performance. The strong signature of parallelism for these phenotypic traits indicates that divergence is likely to be adaptive and is likely to have been driven by differences in predatory regimes. Furthermore, our results indicate that physical performance, behavior and morphology can change rapidly and in concert as new habitats are colonized.

Rapid adaptive divergence between ecotypes of an aquatic isopod inferred from F-Q analysis.

Divergent natural selection is often thought to be the principal factor driving phenotypic differentiation between populations. We studied two ecotypes of the aquatic isopod Asellus aquaticus which have diverged in parallel in several Swedish lakes. In these lakes, isopods from reed belts along the shores colonized new stonewort stands in the centre of the lakes and rapid phenotypic changes in size and pigmentation followed after colonization. We investigated if selection was likely to be responsible for these observed phenotypic changes using indirect inferences of selection (FST–QST analysis). Average QST for seven quantitative traits were higher than the average FST between ecotypes for putatively neutral markers (AFLPs). This suggests that divergent natural selection has played an important role during this rapid diversification. In contrast, the average QST between the different reed ecotype populations was not significantly different from the mean FST. Genetic drift could therefore not be excluded as an explanation for the minor differences between allopatric populations inhabiting the same source habitat. We complemented this traditional FST–QST approach by comparing the FST distributions across all loci (n = 67–71) with the QST for each of the seven traits. This analysis revealed that pigmentation traits had diverged to a greater extent and at higher evolutionary rates than size‐related morphological traits. In conclusion, this extended and detailed type of FST–QST analysis provides a powerful method to infer adaptive phenotypic divergence between populations. However, indirect inferences about the operation of divergent selection should be analyzed on a per‐trait basis and complemented with detailed ecological information.

Phenotypic integration and conserved covariance structure in calopterygid damselflies.

By comparing the phenotypic (P) variance–covariance matrices between closely related taxa or conspecific populations, one can study the outcome of the interplay between selection and developmental constraints in phenotypic evolution. Shared patterns of phenotypic integration are also of interest and might result from similarities in either selection or developmental pathways. We compared P‐matrices and phenotypic integration indices between populations and species of the damselfly genus Calopteryx. Pmax‐comparisons between parapatric C. splendens populations revealed stronger conserved phenotypic covariance structure than Pmax‐comparisons between species, suggesting that divergence in its early stages proceeds along phenotypic lines of least resistance. Within‐ and among‐population correlations in C. splendens were highly concordant, in further support of initial divergence along Pmax. Despite some similarities in overall phenotypic integration between C. splendens and C. virgo, these two species only had several P‐matrix eigenvectors in common, indicating that after reproductive isolation, divergence has proceeded against Pmax.