QTL analysis of a rapidly evolving speciation phenotype in the Hawaiian cricket Laupala

Abstract

In mate recognition systems, the functional necessity to coordinate traits involved in sexual communication should result in reduced pairing potential for new variants outside the distribution of common reproductive signals. Yet, many closely related, sexual species differ in mate recognition traits, suggesting that directional selection influences the divergence of mate recognition systems. Species of the endemic Hawaiian cricket genus Laupala are morphologically and ecologically cryptic, although both male calling song and female acoustic preference have diverged rapidly between closely related species. These mate recognition phenotypes are therefore often likely to be speciation phenotypes, i.e. traits whose divergence contributes, directly or indirectly, to a reduction of gene flow during speciation, given their frequent participation in early lineage divergence. We conducted a replicated, quantitative trait loci (QTL) mapping study of the genetic basis of differences in male calling song between two closely related species, Laupala paranigra and Laupala kohalensis, allowing us to examine the genetic basis of traits involved in rapid speciation. We found statistical support for eight QTL in one replicate, with at least four of these QTL mapping to the same regions in a second replicate. QTL effects ranged between 3.0% and 10.7% of the difference in pulse rate between L. paranigra and L. kohalensis, and are thus of moderate to small effect. All QTL identified show directional effects consistent with the hypothesis of directional selection. Thus, we conclude that rapid speciation can occur under the influence of many genes of moderate to small effect. This study implicates the role of directional selection in the divergence of mate recognition traits and speciation the Hawaiian cricket genus Laupala.

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

“…Previously, the pulse rates of 190 F 2 males from this cross were reported (23) (Fig. 1C), showing a normal distribution between the pulse rates of the 2 parental species (F 2 pulse rate mean Ϯ SD ϭ 1.86 Ϯ 0.36; Shapiro-Wilk: W ϭ 0.994, P ϭ 0.636) (23). (23), equal to the number predicted by cytological analysis (24).…”

“…Male L. kohalensis and L. paranigra songs have pulse rates of 3.72 Ϯ 0.128 pulses per second (pps) and 0.71 Ϯ 0.079 pps, respectively ( Fig. 1 A) (23). Previously, the pulse rates of 190 F 2 males from this cross were reported (23) (Fig.…”

“…Most AFLP markers are dominant, but inclusion of several codominant AFLP markers allowed alignment of the Lp and Lk maps ( Fig. S1) (23). Map size estimates were 613.1 and 476.6 cM, and average marker spacings were 7.5 and 5.8 cM for Lp and Lk, respectively (23).…”

“…We tested the hypothesis of genetic linkage between signal and preference in this system, where both male calling songs and female acoustic preferences have diverged repeatedly (17,(20)(21)(22) and contribute to sexual isolation (15) among closely related species. Laupala species with distinct songs can be hybridized, enabling studies of interspecific genetic architecture (23). Here, we employ a quantitative trait locus (QTL) approach to map female acoustic preference loci that differ between the closely related Laupala paranigra and Laupala kohalensis, and we combine these results with previous QTL work on male calling song differences between these same species (23).…”

Speciation through evolution of sex-linked genes

“…The strikingly rapid (and possibly sympatric) radiation among the Hawaiian Laupala crickets (Mendelson and Shaw, 2005) is probably driven by divergence in calling song and preference (Shaw and Parsons, 2002). By using a combination of QTL studies and investigations of segregation patterns in F2 hybrids between two closely related species of Laupala crickets Shaw et al (2007) found that many genes with small effects were involved in the determination of song and that there was no disproportionate large X effect. To summarize, based on theoretical expectations and on interspecific empirical studies (Table 1) there is more evidence suggesting a large Z effect than a large X effect in the divergence of sexual signalling systems.…”