Behavioral genetics, sexual selection and evolution
Genetic architecture of behavior (QTLs), linkage analysis and genome evolution
Genetics of diverging lineages, speciation and the conceptual nature of species
Molecular systematics (especially of recent groups), comparative methods
The research in my laboratory investigates the nature and origin of species, focusing on genetic and phylogenetic behavioral changes that diverge early in speciation. Current research effort focuses on studies of reproductive behavior and the evolution of mate recognition among closely related species. Investigations of speciation in my laboratory include analyses of species boundaries (through analysis of DNA sequence and phenotypic variation), microevlutionary divergence through local population-level processes, and the genomic and phylogenetic consequences of speciation (through QTL studies of the genetic architecture and phylogenetic patterns of character evolution). Much of our research is focused on the cricket genus Laupala, a system where mate recognition evolution characterizes closely related species, sexual selection is a likely mechanism of early lineage divergence, genetic dissection of mate recognition and related traits is feasible, and phylogenetic replication of the process exists. With 37 species endemic to the Hawaiian archipelago, Laupala offers an exceptional model to test hypotheses regarding the role of mate recognition evolution in speciation.
Species in the genus Laupala possess a simple acoustic system (where, like other acoustic insects, male song attracts females). The pulsed song of males is an example of a classic ultradian biorhythm (with a period < 24 hrs). Females are attracted to these songs. Species of Laupala differ in song pulse rate and acoustic variants can interbreed and hybridize. Song differences and acoustic preferences are underscored by quantitative genetic bases which we are currently analyzing with genomic mapping and quantitative trait locus (QTL) techniques. Our work reveals that different Laupala lineages show repeated episodes of acoustic behavioral evolution on each of the Hawaiian islands, supplying an unprecedented context for evolutionary replication of song and preference evolution and speciation. Moreover, there is a robust geographic pattern in the distribution of species: older lineages correspond to more ancient Hawaiian islands, while more recent lineages correspond to younger islands. Indeed, 7 endemic species of Laupala are present on the youngest island of Hawaii (0-500,000 years old) offering the conditions necessary for new species to form. Furthermore, the same sorts of acoustic factors that differentiate these species are present among different populations of species on the youngest island.
These observations lead to a series of questions, forming our current research goals in this system.
I. What genomic regions and how many loci are involved in mate recognition differences in Laupala?
Are any known candidate genes involved? We are investigating the genetic architecture underlying song and preference behaviors in the cricket Laupala using genetic mapping techniques. The study of this system capitalizes on a behaviorally and neurophysiologically well-studied rhythm; naturally occurring pulse rate variants show a classically quantitative pattern of inheritance, which can be hybridized to produce powerful genetic hybrid designs. With the genome linkage map, we are mapping genomic regions corresponding to loci involved in marked differences in song and preference behaviors. In contrast to the mutational approach taken in model systems, natural populations of Laupala supply the behavioral variants we are studying genetically. Future investigations will involve finer scale mapping strategies to define and characterize quantitative trait loci that underlie variation in song and preference. Several candidate genes have been identified in other systems that could play a role in song production and variation (e.g. the fly period, timeless, cacophony and slowpoke; the mouse clock; and the human erg, involved in cardiac arrhythmia). Collaborations between genes to produce rhythmic neuromuscular behavior are undoubtedly acting in clock-like genetic systems such as cricket song.
II. Has sexual selection acted on rhythmic behaviors such as song and spermatophore production?
We hypothesize that Laupala operates on a resource based courtship system, where males and females engage in courtship for 6-8 hours, during which males sing, and pass spermless spermatophores to females with extraordinary rhythmicity, culminating in a large sperm-filled spermatophore. Females consume each of these spermatophores, and we suspect that they gain nutrition from the matings. Future work in my laboratory aims to demonstrate the necessary components required for sexual selection: (1) variation in behaviors that confer fitness differences such as song and spermatophore production, (2) a heritable basis to that variation, (3) a response to sexual selection on that variation, and (4) the predicted phylogenetic patterns of sexual selection on these behaviors.
III. What are the reproductive and genealogical boundaries in Laupala? Are they sharp or diffuse? Is gene flow within or between species affected by sexual selection on mate recognition phenotypes? Do gene flow boundaries from genomic regions corresponding to song differ from those that do not correspond to song?
We have begun to estimate genealogical relationships among recent species. Molecular phylogenetic data currently suggests extensive hybridization among species of Laupala. Despite this, acoustic variants remain distinct. One of our future goals is to demonstrate the impact that trait evolution has on species boundaries. With DNA sequencing and other molecular marker information, this unprecedented analysis is possible.
Remarkably, there still are no definitive cases of speciation by sexual selection. The features of Laupala exemplify a broad-scale evolutionary pattern among recently evolved species: sexual features evolve early in the speciation process, suggesting their role in promoting diversification. Laupala provides an avenue for molecular dissection of a pervasive speciation mechanism in a valuable natural history context.
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