The Quantitative Genetic Basis of Mating Behavior and Speciation in Drosophila.
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Date
2004-01-12
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Abstract
The widely-accepted Biological Species Concept defines species as populations that are reproductively isolated, i.e. are unable to mate with one another or produce viable and fertile progeny when given the opportunity. Speciation is characterized by the evolution of prezygotic (ethological barriers to interspecific mating) and postzygotic (reduced viability and fertility of interspecific hybrids) reproductive isolating mechanisms. Although recent progress has been made towards understanding the genetic basis of postzygotic isolation, little is known of the genetic architecture of sexual isolation — arguably the most important form of reproductive isolation in animals. In addition, it has not been determined if reproductive isolation occurs due to selection acting on variation within a species or arises from novel mutations. In order to understand how new species arise, the genetic basis of variation in mating behavior within a species, as well as the genetic basis for prezygotic reproductive isolation between species, must be known.
The mating behavior of Drosophila consists of a series of actions that exchange auditory, visual and chemosensory signals between males and females. Although mating behavior has been studied extensively in Drosophila, most known genes affecting mating behavior have been located through the mutation of single genes. The wide range of variation in courtship behavior in natural populations is believed to arise from the joint segregation of multiple quantitative trait loci (QTL) with varying effects that can be influenced by the environment. Here, we identified QTL that affect courtship occurrence, courtship latency, copulation occurrence and copulation latency that segregate between a D. melanogaster strain selected for reduced male mating propensity (2b) and a standard wild-type strain (Oregon-R). Mating behavior was assessed in a population of 98 recombinant inbred lines derived from these two strains and QTL affecting mating behavior were mapped using composite interval mapping. There were four QTL affecting male mating behavior at cytological locations 1A;3E, 57C;57F, 72A;85F and 96F;99A. We used deficiency complementation mapping to map the autosomal QTL with much higher resolution to five QTL at 56F5;56F8, 56F9;57A2, 70E1;71F4, 78C5;79A1, and 96F1;97B1. Quantitative complementation tests performed for 45 positional candidate genes within these intervals revealed seven genes which failed to complement the QTL: eagle, 18 wheeler, Enhancer of split, Polycomb, spermatocyte arrest, l(2)05510 and l(2)k02206. None of these genes have been previously implicated in mating behavior, demonstrating that quantitative analysis of subtle variants can reveal novel pleiotropic effects of key developmental loci on behavior.
In a separate experiment, we mapped QTL contributing to prezygotic reproductive isolation between Drosophila simulans and D. mauritiana. We mapped at least seven QTL affecting discrimination of D. mauritiana females against D. simulans males, three QTL affecting D. simulans male traits against which D. mauritiana</i> females discriminate, and six QTL affecting D. mauritiana male traits against which D. simulans females discriminate. QTL affecting sexual isolation are largely different in males and females and between the two species, and are not preferentially located on the X chromosome. Relatively few QTL with moderate to large effects associated with pre-zygotic isolation facilitates future positional cloning of the underlying genes. In contrast to results for postzygotic isolation, no epistasis was detected between QTL for prezygotic isolation.
Several of the intraspecific D. melanogaster mating behavior QTL overlap those found to affect reproductive isolation between D. simulans and D. mauritiana. Future testing of these positional candidate genes for their effect on reproductive isolation could provide evidence that speciation arises in response to selection acting on naturally-occurring variation in a population.
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reproductive isolation, speciation, mating, drosophila, QTL, quantitative trait loci, courtship, behavior
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Degree
PhD
Discipline
Genetics
