Abstract
An open question in evolutionary biology is the relationship between standing variation for a trait and the variation that leads to interspecific divergence. By identifying loci underlying phenotypic variation in intra- and interspecific crosses we can determine the extent to which polymorphism and divergence are controlled by the same genomic regions. Sexual traits provide abundant examples of morphological and behavioral diversity within and among species, and here we leverage variation in the Drosophila sex comb to address this question. The sex comb is an array of modified bristles or ‘teeth' present on the male forelegs of several Drosophilid species. Males use the comb to grasp females during copulation, and ablation experiments have shown that males lacking comb teeth typically fail to mate. We measured tooth number in >700 genotypes derived from a multiparental advanced-intercross population, mapping three moderate-effect loci contributing to trait heritability. Two quantitative trait loci (QTLs) coincide with previously identified intra- and interspecific sex comb QTL, but such overlap can be explained by chance alone, in part because of the broad swathes of the genome implicated by earlier, low-resolution QTL scans. Our mapped QTL regions encompass 70–124 genes, but do not include those genes known to be involved in developmental specification of the comb. Nonetheless, we identified plausible candidates within all QTL intervals, and used RNA interference to validate effects at four loci. Notably, TweedleS expression knockdown substantially reduces tooth number. The genes we highlight are strong candidates to harbor segregating, functional variants contributing to sex comb tooth number.
Highlights
Understanding the evolutionary and developmental basis of novel morphological, physiological and behavioral traits is a critical problem in genetics
Our goal was to ask whether genomic regions contributing to intraspecific trait variation were consistent with those for interspecific variation mapped in prior studies
The Drosophila Synthetic Population Resource (DSPR) consists of two sets of recombinant inbred lines (RILs), each descended from an advancedgeneration intercross of eight founder lines, seven specific to a panel (A1–A7 or B1–B7) and one common to both panels (AB8)
Summary
Understanding the evolutionary and developmental basis of novel morphological, physiological and behavioral traits is a critical problem in genetics. Such traits can represent fundamental differences between closely related species, and dissecting their genetic and developmental emergence can help to uncover the evolutionary processes that occur during species divergence. One set of models posit that variation is largely a result of intermediate-frequency polymorphisms that are actively maintained in populations by balancing selection (Barton and Keightley, 2002; Turelli and Barton, 2004). These models are consistent with Darwin’s idea that variation between species is an extension of preexisting variation segregating within populations (Darwin, 1859; Lewontin, 1974). One effective way to determine the evolutionary processes acting on complex trait variation is to experimentally identify and characterize the underlying molecular genetic basis of multiple quantitative trait loci (QTLs), identify the genes involved and detect the molecular signatures of specific selective forces at functional loci (Mitchell-Olds et al, 2007)
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