Janette W. Boughman

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.

Divergent sexual selection enhances reproductive isolation in sticklebacks

Sexual selection may facilitate speciation because it can cause rapid evolutionary diversification of male mating signals and female preferences. Divergence in these traits can then contribute to reproductive isolation. The sensory drive hypothesis predicts that three mechanisms underlie divergence in sexually selected traits: (1) habitat-specific transmission of male signals; (2) adaptation of female perceptual sensitivity to local ecological conditions; and (3) matching of male signals to female perceptual sensitivity. I test these mechanisms in threespine sticklebacks (Gasterosteus spp.) that live in different light environments. Here I show that female perceptual sensitivity to red light varies with the extent of redshift in the light environment, and contributes to divergent preferences. Male nuptial colour varies with environment and is tuned to female perceptual sensitivity. The extent of divergence among populations in both male signal colour and female preference for red is correlated with the extent of reproductive isolation in these recently diverged species. These results demonstrate that divergent sexual selection generated by sensory drive contributes to speciation.

How sensory drive can promote speciation

Abstract Some of the most spectacular and diverse traits in animals are the signals used to attract mates. Closely related species often differ dramatically in signaling traits, in spite of similarity in other morphological traits. The idea that reproductive isolation arises when male mating signals and female preferences differ among populations is an old one. However, until recently, there was almost no information on what generates diversity in mating signals and preferences. This is beginning to change, with emerging results that highlight the importance of habitat differences in generating this diversity. Such differences in ecology are at the root of one hypothesis for divergence in sexual signaling – sensory drive. The sensory drive hypothesis focuses on how communication systems adapt to local environments and predicts that divergence in communication systems will occur when environments differ. Reproductive isolation can arise as a byproduct of this adaptive divergence in behavior.

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.

Speciation in reverse: morphological and genetic evidence of the collapse of a three‐spined stickleback (Gasterosteus aculeatus) species pair

Historically, six small lakes in southwestern British Columbia each contained a sympatric species pair of three‐spined sticklebacks (Gasterosteus aculeatus). These pairs consisted of a ‘benthic’ and ‘limnetic’ species that had arisen postglacially and, in four of the lakes, independently. Sympatric sticklebacks are considered biological species because they are morphologically, ecologically and genetically distinct and because they are strongly reproductively isolated from one another. The restricted range of the species pairs places them at risk of extinction, and one of the pairs has gone extinct after the introduction of an exotic catfish. In another lake, Enos Lake, southeastern Vancouver Island, an earlier report suggested that its species pair is at risk from elevated levels of hybridization. We conducted a detailed morphological analysis, as well as genetic analysis of variation at five microsatellite loci for samples spanning a time frame of 1977 to 2002 to test the hypothesis that the pair in Enos Lake is collapsing into a hybrid swarm. Our morphological analysis showed a clear breakdown between benthics and limnetics. Bayesian model‐based clustering indicated that two morphological clusters were evident in 1977 and 1988, which were replaced by 1997 by a single highly variable cluster. The most recent 2000 and 2002 samples confirm the breakdown. Microsatellite analysis corroborated the morphological results. Bayesian analyses of population structure in a sample collected in 1994 indicated two genetically distinct populations in Enos Lake, but only a single genetic population was evident in 1997, 2000, and 2002. In addition, genetic analyses of samples collected in 1997, 2000, and 2002 showed strong signals of ‘hybrids’; they were genetically intermediate to parental genotypes. Our results support the idea that the Enos Lake species pair is collapsing into a hybrid swarm. Although the precise mechanism(s) responsible for elevated hybridization in the lake is unknown, the demise of the Enos Lake species pair follows the appearance of an exotic crayfish, Pascifasticus lenisculus, in the early 1990s.

Vocal learning by greater spear–nosed bats

Vocal learning is well known among passerine and psittacine birds, but most data on mammals are equivocal. Specific benefits of vocal learning are poorly understood for most species. One case where vocal learning should be favoured by selection is where calls indicate group membership and group mates are unrelated. Female greater spear–nosed bats, Phyllostomus hastatus, live in stable groups of unrelated bats and use loud, broadband calls to coordinate foraging movements of social group mates. Bats benefit from group foraging. Calls differ between female social groups and cave colonies, and playback experiments demonstrate that bats perceive these acoustic differences. Here I show that the group distinctive structure of calls arises through vocal learning. Females change call structure when group composition changes, resulting in increased similarity among new social group mates. Comparisons of transfers with age–matched half–sibs indicate that call changes are not simply due to maturation, the physical environment or heredity. These results suggest that studies testing vocal learning in mammals could profit by focusing on vocalizations that signify group membership.

Greater spear-nosed bats discriminate group mates by vocalizations

Individuals often benefit from identifying their prospective social partners. Some species that live in stable social groups discriminate between their group mates and others, basing this distinction on calls that differ among individuals. Vocalizations that differ between social groups are much less common, and few studies have demonstrated that animals use group-distinctive calls to identify group mates. Female greater spear-nosed bats, Phyllostomus hastatus, live in stable groups of unrelated bats and give audible frequency, broadband calls termed screech calls when departing from the roost and at foraging sites. Previous field observations suggested that bats give screech calls to coordinate movements among group members. Prior acoustic analyses of 12 acoustic variables found group differences but not individual differences. Here, we use the same acoustic variables to compare calls from three cave colonies, and find that calls differ between caves. We also report results from field and laboratory playback experiments designed to test whether bats use acoustic differences to discriminate calls from different colonies, groups or individuals. Results from field playbacks indicate that response depends on the cave of origin, indicating that bats can discriminate among calls from different caves. This discrimination ability may be based, in part, on whether calls are familiar or unfamiliar to the listening bats. Laboratory playbacks demonstrate that bats discriminate calls given by their group mates from calls given by other bats from the same cave irrespective of familiarity. However, these experiments provide no evidence that bats discriminate among individuals. Previous field work indicates that females that forage with social group mates may benefit from shared information about food or mutual defence of feeding sites. Indicating group membership is essential, since these benefits appear to be restricted to group mates. Copyright 1998 The Association for the Study of Animal Behaviour. Copyright 1998 The Association for the Study of Animal Behaviour.

Greater spear-nosed bats give group-distinctive calls

Abstract Individually distinctive vocalizations are ubiquitous; however, group distinctive calls have rarely been demonstrated. Under some conditions, selection should favor calls indicating social group membership in animals that forage in groups. Greater spear-nosed bats (Phyllostomus hastatus) give calls that appear to facilitate recognition of social group mates who are unrelated. Females give loud broadband (4–18 kHz) vocalizations termed screech calls when departing on foraging trips and at foraging sites. Screech calls help to establish foraging groups among social group members, and to maintain contact over the long distances they travel while foraging. I test two hypotheses about how screech calls may be structured to convey caller identity. Individual calls may be distinct and group members may learn to recognize each individuals calls and to associate the individual with the social group. Alternatively, groups may give distinct calls and individuals within groups may share call characteristics. To test these hypotheses I conducted multivariate acoustic analysis of multiple calls from 28 bats from three social groups. Although the ubiquity of individually distinctive calls in other taxa makes this result more likely, the results reveal that group calls are highly distinctive. Individual bats within groups are statistically indistinguishable. Calls appear to decrease slightly in frequency as bats age. Call convergence among unrelated group mates implies vocal learning in this species.

Sexual imprinting on ecologically divergent traits leads to sexual isolation in sticklebacks

During sexual imprinting, offspring learn parental phenotypes and then select mates who are similar to their parents. Imprinting has been thought to contribute to the process of speciation in only a few rare cases; this is despite imprintings potential to generate assortative mating and solve the problem of recombination in ecological speciation. If offspring imprint on parental traits under divergent selection, these traits will then be involved in both adaptation and mate preference. Such ‘magic traits’ easily generate sexual isolation and facilitate speciation. In this study, we show that imprinting occurs in two ecologically divergent stickleback species (benthics and limnetics: Gasterosteus spp.). Cross-fostered females preferred mates of their foster fathers species. Furthermore, imprinting is essential for sexual isolation between species; isolation was reduced when females were raised without fathers. Daughters imprinted on father odour and colour during a critical period early in development. These traits have diverged between the species owing to differences in ecology. Therefore, we provide the first evidence that imprinting links ecological adaptation to sexual isolation between species. Our results suggest that imprinting may facilitate the evolution of sexual isolation during ecological speciation, may be especially important in cases of rapid diversification, and thus play an integral role in the generation of biodiversity.

Breakdown in postmating isolation and the collapse of a species pair through hybridization.

Species that evolved through ecological speciation and that lack intrinsic genetic incompatibilities may nonetheless be maintained by extrinsic postmating isolating barriers that impose selection against hybrids. These species, however, may be vulnerable to a breakdown in postmating isolation. Here, we investigate a model system for ecological speciation: sympatric limnetic‐benthic pairs of threespine sticklebacks. Recently, stickleback hybrid abundance in Enos Lake has increased. Given that ecological selection against hybrids was historically an important component of total reproductive isolation, we tested whether ecologically dependent postmating isolation is still functioning. We compared body shape, diet, growth, and survival in present‐day Enos fish with trait data in the undisturbed Paxton Lake species pair and with historical Enos Lake data. In both Paxton and historical Enos data, we found a strong correlation between body shape and diet; however, in present‐day Enos fish, this correlation was absent. Using fitness estimates based on growth rates and survival, we found no evidence of selection against intermediate morphologies. It appears that postmating isolation has broken down, allowing hybrids to persist and contributing to the collapse of the species pair.