Tamra C. Mendelson

Sexual behaviour: Rapid speciation in an arthropod

Theory predicts that sexual behaviour in animals can evolve rapidly, accelerating the rate of species formation. Here we estimate the rate of speciation in Laupala, a group of forest-dwelling Hawaiian crickets that is characterized primarily through differences in male courtship song. We find that Laupala has the highest rate of speciation so far recorded in arthropods, supporting the idea that divergence in courtship or sexual behaviour drives rapid speciation in animals.

Contributions of natural and sexual selection to the evolution of premating reproductive isolation: a research agenda.

Speciation by divergent natural selection is well supported. However, the role of sexual selection in speciation is less well understood due to disagreement about whether sexual selection is a mechanism of evolution separate from natural selection, as well as confusion about various models and tests of sexual selection. Here, we outline how sexual selection and natural selection are different mechanisms of evolutionary change, and suggest that this distinction is critical when analyzing the role of sexual selection in speciation. Furthermore, we clarify models of sexual selection with respect to their interaction with ecology and natural selection. In doing so, we outline a research agenda for testing hypotheses about the relative significance of divergent sexual and natural selection in the evolution of reproductive isolation.

RAPID EVOLUTION OF CUTICULAR HYDROCARBONS IN A SPECIES RADIATION OF ACOUSTICALLY DIVERSE HAWAIIAN CRICKETS (GRYLLIDAE: TRIGONIDIINAE: LAUPALA)

Abstract Understanding the origin and maintenance of barriers to gene exchange is a central goal of speciation research. Hawaiian swordtail crickets (genus Laupala) represent one of the most rapidly speciating animal groups yet identified. Extensive acoustic diversity, strong premating isolation, and female preference for conspecific acoustic signals in laboratory phonotaxis trials have strongly supported divergence in mate recognition as the driving force behind the explosive speciation seen in this system. However, recent work has shown that female preference for conspecific male calling song does not extend to mate choice at close range among these crickets, leading to the hypothesis that additional sexual signals are involved in mate recognition and premating isolation. Here we examine patterns of variation in cuticular lipids among several species of Laupala from Maui and the Big Island of Hawaii. Results demonstrate (1) a rapid and dramatic evolution of cuticular lipid composition among species in this genus, (2) significant differences among males and females in cuticular lipid composition, and (3) a significant reduction in the complexity of cuticular lipid profiles in species from the Big Island of Hawaii as compared to two outgroup species from Maui. These results suggest that behavioral barriers to gene exchange in Laupala may be composed of multiple mate recognition signals, a pattern common in other cricket species.

THE ACCUMULATION OF REPRODUCTIVE BARRIERS DURING SPECIATION: POSTMATING BARRIERS IN TWO BEHAVIORALLY ISOLATED SPECIES OF DARTERS (PERCIDAE: ETHEOSTOMA)

Abstract Identifying the manner in which reproductive barriers accumulate during lineage divergence is central to establishing general principles of species formation. One outstanding question is which isolating mechanisms form the first complete barrier to gene flow in a given lineage or under a particular set of conditions. To identify these initial reproductive barriers requires examining lineages in very early stages of divergence, before multiple reproductive barriers have evolved to completion. We quantified the strength of three postmating barriers in a pair of darter species and compared these estimates to each other and to the strength of behavioral isolation (BI) reported in a previous study. Results reveal no evidence of gametic incompatibility but intermediate levels of conspecific sperm precedence and hybrid inviability. As BI is nearly complete, our analysis comparing the strength of multiple reproductive barriers implicates the evolution of mate choice as central to both the origin and maintenance of these species. Further examination of ecological isolation and hybrid sterility is necessary to determine the role of these barriers in darter speciation.

Genetic and Behavioral Components of the Cryptic Species Boundary between Laupala Cerasina and L. Kohalensis (Orthoptera: Gryllidae)

Cryptic species are often hypothesized on the basis of differences in courtship signals. These signal differences suggest that mate recognition systems, which include both courtship signals and responses to those signals, have diverged between genetically isolated populations. Cryptic species are therefore thought to represent distinct genetic units, the boundaries of which are maintained by premating incompatibilities, specifically by receiver preferences for conspecific signals. Laupala cerasina and L. kohalensis are sympatric species of swordtail crickets endemic to the big island of Hawaii, that are distinguishable by differences in male courtship song. We first tested whether groupings hypothesized by acoustic similarity reflect genetic groupings, using AFLP data to estimate genetic relationships. Second, we tested whether genetic boundaries are maintained by female preferences for conspecific song characteristics. Phonotaxis trials were used to determine the extent of female preferences for conspecific male song. Results generally support both hypotheses, but suggest the presence of porous species boundaries.

Female preference for male coloration may explain behavioural isolation in sympatric darters

Animal colour patterns are among the most striking examples of biological diversity. Elaborate coloration is thought to play a role in mate choice within populations and to pose a barrier to interbreeding between species, with individuals preferring the coloration of conspecifics. Ideally, the importance of coloration as a reproductive barrier would be tested by holding all traits constant and manipulating only colour to test its effect. In butterflies, researchers use paper models to manipulate female colour patterns and show strong male preference for conspecific female coloration. In African cichlids and poison frogs, researchers manipulate the light environment to test the importance of male colour in female preference for conspecifics. Here we use motorized models to test whether females in a pair of sexually dimorphic fish species (genus: Etheostoma ) prefer conspecific over heterospecific male coloration. By isolating and manipulating specific components of male coloration, we show that females of both species significantly prefer conspecific male colour (red versus green) and pattern (stripe versus bars). These results provide strong evidence that female preference for conspecific male nuptial coloration may play a critical role in behavioural isolation.

Cx23, a connexin with only four extracellular-loop cysteines, forms functional gap junction channels and hemichannels

Gap junction channels may be comprised of either connexin or pannexin proteins (innexins and pannexins). Membrane topologies of both families are similar, but sequence similarity is lacking. Recently, connexin‐like sequences have been identified in mammalian and zebrafish genomes that have only four conserved cysteines in the extracellular domains (Cx23), a feature of the pannexins. Phylogenetic analyses of the non‐canonical “C4” connexins reveal that these sequences are indeed connexins. Functional assays reveal that the Cx23 gap junctions are capable of sharing neurobiotin, and further, that Cx23 connexins form hemichannels in vitro.

Use of AFLP Markers in Surveys of Arthropod Diversity

Arthropods comprise the most diverse group of animals on earth and as such have been the subject of considerable evolutionary research. For example, much of our understanding of the genetic basis of evolutionary change is derived from the insect genus Drosophila, one of the most well-studied organisms in biology. Arthropods are also of tremendous economic importance as both providers and chief destroyers of food for human consumption. Thus, the genetic diversity of arthropods is of interest from both a pure research perspective and for practical economic reasons. The amplified fragment length polymorphism (AFLP) method of genetic analysis, developed in the early and mid-1990s (Vos et al., 1995; Zabeau, 1992; Zabeau and Vos, 1993), offers a relatively new method for assessing genetic diversity and has been increasingly applied in studies of arthropods. Originally coined selective restriction fragment amplification (SRFA) (Zabeau and Vos, 1993), the method was renamed (Vos et al., 1995) presumably to reflect its similarity to restriction fragment length polymorphism (RFLP). Since then, AFLPs have become a popular tool in both population genetics to estimate population parameters such as heterozygosity, F-statistics, migration rates, and genetic distances, as well as phylogenetics, to infer relationships among closely related taxa. In arthropods, AFLPs have been used to assess genetic variation both within and between species in various taxa including crustaceans, chelicerates, and insects, often yielding novel insights. In this chapter, we briefly describe the AFLP method and its strengths and limitations. We then discuss the use of AFLPs in surveys of arthropod diversity, highlighting the specific questions addressed using AFLPs. Finally, a section on experimental design and methods, based on research in our laboratory, is provided.

Quantifying patterns in the evolution of reproductive isolation.

Abstract We present a likelihood‐based statistical method for examining the pattern or rate of evolution of reproductive isolation. The method uses large empirical datasets to estimate, for a given clade, the average duration of two phases in the divergence of populations. The first phase is a lag phase and refers to the period during which lineages diverge but no detectable reproductive isolation evolves. The second is an accumulation phase, referring to the period during which the magnitude of reproductive isolation between diverging lineages increases. The pattern of evolution is inferred from the relative durations of these two phases. Results of analyses of postzygotic isolation data indicate significant differences among taxa in the pattern of evolution of postzygotic isolation that are consistent with predictions based on genetic differences among these groups. We also examine whether the evolution of postzygotic isolation is best explained by either of two models for the rate of accumulation: a linear model or a quadratic function as may be suggested by recent studies. Our analysis indicates that the appropriateness of either model varies among taxa.

Epigenetic divergence as a potential first step in darter speciation

Recent studies show that epigenetic variation in the form of DNA methylation may serve as a substrate for selection. Theory suggests that heritable epigenetic marks that increase fitness should increase in frequency in a population, and these changes may result in novel morphology, behaviour, or physiology, and ultimately reproductive isolation. Therefore, epigenetic variation might provide the first substrate for selection during the course of evolutionary divergence. This hypothesis predicts that populations in the earliest stages of divergence will differentiate in their methylome prior to any genetic differentiation. While several studies have investigated natural epigenetic variation, empirical studies that test predictions about its role in speciation are surprisingly scarce. Here, we investigate DNA methylation variation using an isoschizomeric digest method, Methyl‐Sensitive Amplified Polymorphism, across multiple stages of evolutionary divergence in natural populations of North American stream fishes. We show that epigenetic differentiation between methylomes is greater than genetic divergence among closely related populations across two river drainages. Additionally, we demonstrate that epigenetic divergence is a stronger predictor of the strength of behavioural reproductive isolation and suggest that changes in the methylome could influence the evolution of reproductive isolation between species. Our findings suggest a role for epigenetics not only in the initiation of divergence, but also in the maintenance of species boundaries over greater evolutionary timescales.