Kerry L. Shaw

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.

A Genealogical Approach to Quantifying Lineage Divergence

Abstract We introduce a statistic, the genealogical sorting index (gsi), for quantifying the degree of exclusive ancestry of labeled groups on a rooted genealogy and demonstrate its application. The statistic is simple, intuitive, and easily calculated. It has a normalized range to facilitate comparisons among different groups, trees, or studies and it provides information on individual groups rather than a composite measure for all groups. It naturally handles polytomies and accommodates measures of uncertainty in phylogenetic relationships. We use coalescent simulations to explore the behavior of the gsi across a range of divergence times, with the mean value increasing to 1, the maximum value when exclusivity within a group reached monophyly. Simulations also demonstrate that the power to reject the null hypothesis of mixed genealogical ancestry increased markedly as sample size increased, and that the gsi provides a statistically more powerful measure of divergence than FST. Applications to data from published studies demonstrated that the gsi provides a useful way to detect significant exclusivity even when groups are not monophyletic. Although we describe this statistic in the context of divergence, it is more broadly applicable to quantify and assess the significance of clustering of observations in labeled groups on any tree.

Species boundaries and genetic diversity among Hawaiian crickets of the genus Laupala identified using amplified fragment length polymorphism

Crickets of the genus Laupala represent one of the many morphologically cryptic groups of insects, with the most closely related species distinguished only by the male calling song. Cryptic groups provide a challenge in determining the genetic boundaries between closely related populations and species. We have addressed the question of species boundaries in the Hawaiian cricket, Laupala, using nuclear DNA patterns sampled by the amplified fragment length polymorphism (AFLP) technique. This method has been used widely by plant researchers to facilitate the rapid assessment of genetic diversity in very closely related species and varieties. The AFLP technique is simple and robust, can be applied to any organism, and overcomes problems associated with cost, development time, information content and reproducibility that can plague other marker systems. Our results support previously hypothesized taxonomic relationships among sympatric populations and suggest close genetic relationships among allopatric, conspecific populations.

The (mis)concept of species recognition

To many, the concept of species recognition is integral to the origin and maintenance of species. However, the heuristic value of species recognition is hampered by its reliance on the problematic concept of species. In this paper, we first discuss assumptions associated with prevailing use of the term, including the typological implications of the concept, the false dichotomy of compatibility and mate quality, and the commonly held model of species recognition in which animals determine taxonomic status before mate status. Subsequently, we propose research directions aimed to improve our understanding of the role of courtship behavior in speciation. We propose two complementary research approaches, one addressing the processes that drive the evolution of mate recognition systems and the other addressing the phenotypic architecture of behavioral isolation. Our approach emphasizes the fitness consequences and multidimensional nature of mate choice.

POLYGENIC INHERITANCE OF A BEHAVIORAL PHENOTYPE: INTERSPECIFIC GENETICS OF SONG IN THE HAWAIIAN CRICKET GENUS LAUPALA

The Hawaiian cricket genus Laupala (family Gryllidae) is one of several native genera of flightless crickets found in rain‐forest habitat across the Hawaiian archipelago. Species in this genus are morphologically quite similar, but the songs produced by adult males are acoustically distinct. I examined the nature of song variation found within Laupala paranigra and between Laupala kohalensis and L. paranigra, both endemic to the island of Hawaii. Variation within and among species was most notable in the temporal structure of the song, as quantified by the pulse rate. The variation in pulse rate present in natural populations of L. paranigra bred true through the F1 laboratory generation, suggesting that the intraspecific variation in this species has a genetic basis. Interspecific hybridizations between L. kohalensis and L. paranigra successfully produced F1, F2, and backcross generations. Hybrid F1 males from reciprocal crosses sang with significantly different pulse rates, implicating an X chromosomal contribution to the phenotypic difference between these species. Interspecific patterns of inheritance are most consistent with a type‐I genetic architecture. Polygenic inheritance of the interspecific pulse‐rate variation was observed, and approximately eight genetic factors were estimated to underlie the difference in pulse rate between L. kohalensis and L. paranigra.

SEQUENTIAL RADIATIONS AND PATTERNS OF SPECIATION IN THE HAWAIIAN CRICKET GENUS LAUPALA INFERRED FROM DNA SEQUENCES

The tremendous diversity of endemic Hawaiian crickets is thought to have originated primarily through intraisland radiations, in contrast to an interisland mode of diversification in the native Hawaiian Drosophila. The Hawaiian cricket genus Laupala (family Gryllidae) is one of several native genera of flightless crickets found in rain‐forest habitat across the Hawaiian archipelago. I examined the phylogenetic relationships among mitochondrial DNA (mtDNA) sequences sampled from 17 species of Laupala, including the 12S ribosomal RNA (rRNA), transfer RNA (RNA)val and 16S rRNA regions. The distribution of mtDNA variants suggests that species within Laupala are endemic to single islands. The phylogenetic estimate produced from both maximum likelihood and maximum parsimony supports the hypothesis that speciation in Laupala occurred mainly within islands. The inferred biogeographical history suggests that diversification in Laupala began on Kauai, the oldest rain‐forested Hawaiian island. Subsequently, colonization to younger islands in the archipelago resulted in a radiation of considerable phylogenetic diversity. Phylogenetic patterns in mtDNA are not congruent with prior systematic or taxonomic hypotheses. Hypotheses that may explain the conflict between the phylogenetic patterns of mtDNA variation and the species taxonomy are discussed.

INTERSPECIFIC GENETICS OF MATE RECOGNITION: INHERITANCE OF FEMALE ACOUSTIC PREFERENCE IN HAWAIIAN CRICKETS

Abstract. Female mating behavior plays a fundamental role in the divergent evolution of mate recognition systems that may lead to speciation. Despite this important role, the phenotypic and genetic bases of female mating behavior remain poorly understood. In this study, I examine the shape of the female acoustic preference function and estimate values for pulse rate preference in two species of Hawaiian crickets, Laupala kohalensis and L. paranigra. In addition, I examine how preference differences are inherited in hybrid crosses between these species. Females expressed unimodal preference functions and were generally more attracted to pulse rates characterizing their own species. Unimodal preference functions also characterized F1 and backcross generations, with hybrid females expressing preferences for intermediate pulse rates. Pulse rate preferences segregated in the backcross generation. Mean pulse rate preference matched mean pulse rate in both parental and hybrid generations. Based on F1 hybrids and segregation patterns in backcross females, I show that changes in both signal and receiver components of the mate recognition system are consistent with a multilocus model of change through incremental steps. The results therefore suggest that ancestors of the current species also expressed unimodal preference functions and that changes in acoustic communication signals occurred through shifts in mean pulse rates and pulse rate preferences among populations.

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.

Genomic linkage of male song and female acoustic preference QTL underlying a rapid species radiation

The genetic coupling hypothesis of signal-preference evolution, whereby the same genes control male signal and female preference for that signal, was first inspired by the evolution of cricket acoustic communication nearly 50 years ago. To examine this hypothesis, we compared the genomic location of quantitative trait loci (QTL) underlying male song and female acoustic preference variation in the Hawaiian cricket genus Laupala. We document a QTL underlying female acoustic preference variation between 2 closely related species (Laupala kohalensis and Laupala paranigra). This preference QTL colocalizes with a song QTL identified previously, providing compelling evidence for a genomic linkage of the genes underlying these traits. We show that both song and preference QTL make small to moderate contributions to the behavioral difference between species, suggesting that divergence in mating behavior among Laupala species is due to the fixation of many genes of minor effect. The diversity of acoustic signaling systems in crickets exemplifies the evolution of elaborate male displays by sexual selection through female choice. Our data reveal genetic conditions that would enable functional coordination between song and acoustic preference divergence during speciation, resulting in a behaviorally coupled mode of signal-preference evolution. Interestingly, Laupala exhibits one of the fastest rates of speciation in animals, concomitant with equally rapid evolution in sexual signaling behaviors. Genomic linkage may facilitate rapid speciation by contributing to genetic correlations between sexual signaling behaviors that eventually cause sexual isolation between diverging populations.

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.