Contemporary ecotypic divergence during a recent range expansion was facilitated by adaptive introgression

Although rapid phenotypic evolution during range expansion associated with colonization of contrasting habitats has been documented in several taxa, the evolutionary mechanisms that underlie such phenotypic divergence have less often been investigated. A strong candidate for rapid ecotype formation within an invaded range is the three-spine stickleback in the Lake Geneva region of central Europe. Since its introduction only about 140 years ago, it has undergone a significant expansion of its range and its niche, now forming phenotypically differentiated parapatric ecotypes that occupy either the pelagic zone of the large lake or small inlet streams, respectively. By comparing museum collections from different times with contemporary population samples, we here reconstruct the evolution of parapatric phenotypic divergence through time. Using genetic data from modern samples, we infer the underlying invasion history. We find that parapatric habitat-dependent phenotypic divergence between the lake and stream was already present in the first half of the twentieth century, but the magnitude of differentiation increased through time, particularly in antipredator defence traits. This suggests that divergent selection between the habitats occurred and was stable through much of the time since colonization. Recently, increased phenotypic differentiation in antipredator defence traits likely results from habitat-dependent selection on alleles that arrived through introgression from a distantly related lineage from outside the Lake Geneva region. This illustrates how hybridization can quickly promote phenotypic divergence in a system where adaptation from standing genetic variation was constrained

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

Background: Clear 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. Results: Contrary 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. Conclusion: Our 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

The genetics of mate preferences in hybrids between two young and sympatric Lake Victoria cichlid species

The genetic architecture of mate preferences is likely to affect significant evolutionary processes, including speciation and hybridization. Here, we investigate laboratory hybrids between a pair of sympatric Lake Victoria cichlid fish species that appear to have recently evolved from a hybrid population between similar predecessor species. The species demonstrate strong assortative mating in the laboratory, associated with divergent male breeding coloration (red dorsum versus blue). We show in a common garden experiment, using DNA-based paternity testing, that the strong female mate preferences among males of the two species are fully recovered in a large fraction of their F2 hybrid generation. Individual hybrid females often demonstrated consistent preferences in multiple mate choice trials (more than or equal to five) across a year or more. This result suggests that female mate preference is influenced by relatively few major genes or genomic regions. These preferences were not changed by experience of a successful spawning event with a male of the non-preferred species in a no-choice single-male trial. We found no evidence for imprinting in the F2 hybrids, although the F1 hybrid females may have been imprinted on their mothers. We discuss this nearly Mendelian inheritance of consistent innate mate preferences in the context of speciation theory

Habitat choice and female preference in a polymorphic stickleback population

Background: A small pond, c. 90 years old, near Bern, Switzerland contains a population of threespine stickleback (Gasterosteus aculeatus) with two distinct male phenotypes. Males of one type are large, and red, and nest in the shallow littoral zone. The males of the other are small and orange, and nest offshore at slightly greater depth. The females in this population are phenotypically highly variable but cannot easily be assigned to either male type. Question: Is the existence of two sympatric male morphs maintained by substrate-associated male nest site choice and facilitated by female mate preferences? Organisms: Male stickleback caught individually at their breeding sites. Females caught with minnow traps. Methods: In experimental tanks, we simulated the slope and substrate of the two nesting habitats. We then placed individual males in a tank and observed in which habitat the male would build his nest. In a simultaneous two-stimulus choice design, we gave females the choice between a large, red male and a small, orange one. We measured female morphology and used linear mixed effect models to determine whether female preference correlated with female morphology. Results: Both red and orange males preferred nesting in the habitat that simulated the slightly deeper offshore condition. This is the habitat occupied by the small, orange males in the pond itself. The proportion of females that chose a small orange male was similar to that which chose a large red male. Several aspects of female phenotype correlated with the male type that a female preferred

Temporally consistent species differences in parasite infection but no evidence for rapid parasite-mediated speciation in Lake Victoria cichlid fish

Abstract Parasites may have strong eco-evolutionary interactions with their hosts. Consequently, they may contribute to host diversification. The radiation of cichlid fish in Lake Victoria provides a good model to study the role of parasites in the early stages of speciation. We investigated patterns of macroparasite infection in a community of 17 sympatric cichlids from a recent radiation and 2 older species from 2 non-radiating lineages, to explore the opportunity for parasite-mediated speciation. Host species had different parasite infection profiles, which were only partially explained by ecological factors (diet, water depth). This may indicate that differences in infection are not simply the result of differences in exposure, but that hosts evolved species-specific resistance, consistent with parasite-mediated divergent selection. Infection was similar between sampling years, indicating that the direction of parasite-mediated selection is stable through time. We morphologically identified 6 Cichlidogyrus species, a gill parasite that is considered a good candidate for driving parasite-mediated speciation, because it is host species-specific and has radiated elsewhere in Africa. Species composition of Cichlidogyrus infection was similar among the most closely related host species (members of the Lake Victoria radiation), but two more distantly related species (belonging to non-radiating sister lineages) showed distinct infection profiles. This is inconsistent with a role for Cichlidogyrus in the early stages of divergence. To conclude, we find significant interspecific variation in parasite infection profiles, which is temporally consistent. We found no evidence that Cichlidogyrus-mediated selection contributes to the early stages of speciation. Instead, our findings indicate that species differences in infection accumulate after speciation.Peer reviewe

Signals of predation-induced directional and disruptive selection in the threespine stickleback

Background: Different predation regimes may exert divergent selection pressure on phenotypes and their associated genotypes. Threespine stickleback Gasterosteus aculeatus have a suite of bony structures, which have been shown to be an effective defence against predation and have a well-known genetic basis. Question: Do different predator regimes induce different selective pressures on growth rates and defence phenotypes in threespine stickleback between different habitats across distinct age classes? Hypothesis: In the presence of predation-induced selection, we expect diverging morphological responses between populations experiencing either low or high predation pressure. Study system: Threespine stickleback were sampled from two natural but recently established populations in an invasive range. One site has a high density of fish and insect predators, while at the other site predation pressure is low. Methods: We inferred predator-induced selection on defence traits by comparing the distribution of size classes, defence phenotypes, and an armour-related genotype between different age classes in a high and a low predation regime. Results: Under high predation, there are indications of directional selection for faster growth, whereas lateral plate phenotypes and associated genotypes show indications for disruptive selection. Heterozygotes at the Eda-gene have a lower survival rate than either homozygote. Neither pattern is evident in the low predation regime. Conclusion: Potential evolutionary responses to divergent predation pressures between sites are apparent in a recently established system