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. 2009 Jun 16;106(24):9737-42.
doi: 10.1073/pnas.0900229106. Epub 2009 Jun 1.

Genomic Linkage of Male Song and Female Acoustic Preference QTL Underlying a Rapid Species Radiation

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Free PMC article

Genomic Linkage of Male Song and Female Acoustic Preference QTL Underlying a Rapid Species Radiation

Kerry L Shaw et al. Proc Natl Acad Sci U S A. .
Free PMC article

Abstract

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.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Geographic range and male pulse rate variation of L. paranigra, L. kohalensis, and F1 hybrids (A) (23); F2 hybrid female pulse rate preference variation (B); and F2 hybrid male pulse rate variation (C) (23).
Fig. 2.
Fig. 2.
QTL scans of interspecific song and preference variation on Lp (A) and Lk (B) linkage maps. Horizontal bars, with tick marks indicating AFLP marker locations, represent linkage maps. Orthology between Lk and Lp linkage groups was previously established (Fig. S1) (23). LOD traces are CIM QTL scans based on multiple imputation with a window size of 20 cM (Lp song and preference, Lk song), and IM QTL scan (Lk preference). Asterisks indicate background markers used as covariates in CIM analyses, and dashed horizontal lines indicate 5% LOD significance thresholds based on permutation. Light and dark gray vertical bars indicate the 1.5 LOD significance thresholds for location of preference and corresponding pulse rate QTL, respectively. [Reproduced with permission from ref. (Copyright 2007, Wiley-Blackwell).]

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