The Genetics of Mating Song Evolution Underlying Rapid Speciation: Linking Quantitative Variation to Candidate Genes for Behavioral Isolation

Abstract

Differences in mating behaviors evolve early during speciation, eventually contributing to reproductive barriers between species. Knowledge of the genetic and genomic basis of these behaviors is therefore integral to a causal understanding of speciation. Acoustic behaviors are often part of the mating ritual in animal species. The temporal rhythms of mating songs are notably speciesspecific in many vertebrates and arthropods and often underlie assortative mating. Despite discoveries of mutations that disrupt the temporal rhythm of these songs, we know surprisingly little about genes affecting naturally occurring variation in the temporal pattern of singing behavior. In the rapidly speciating Hawaiian cricket genus Laupala, the striking species variation in song rhythms constitutes a behavioral barrier to reproduction between species. Here, we mapped the largest-effect locus underlying interspecific variation in song rhythm between two Laupala species to a narrow genomic region, wherein we find no known candidate genes affecting song temporal rhythm in Drosophila. Whole-genome sequencing, gene prediction, and functional annotation of this region reveal an exciting and promising candidate gene, the putative cyclic nucleotide-gated ion channel-like gene, for natural variation in mating behavior, suggesting that ion channels are important targets of selection on rhythmic signaling during establishment of behavioral isolation and rapid speciation.

Genetic coupling of signal and preference facilitates sexual isolation during rapid speciation

“…2, Supplementary Fig. 2, Table 1), consistent with previous results 39 . The 1.5-LOD confidence interval of this QTL spanned 0.46 cM (Table 1, Fig.…”

“…The phenotypic effect of an allele at the pulse rate QTL was almost entirely additive (0.33 ± 0.01 pps), explaining 11.0% of species difference (Table 1). The F 2 phenotypic distribution of male pulse rate was consistent with a 1:2:1 segregation ratio as shown previously 39 and did not significantly differ from that of female preference in F 2 (X 2 = 2.15, df = 2, p = 0.34).…”

“…We used pulse rate measures from 339 and 130 males in 4C.9 and 4E.1 respectively (published previously in 39 ). A major-effect QTL explaining 85.6% F 2 variance in pulse rate was localized at 26.40 cM in both IMP and MQM (Fig.…”

“…Here we show that the highest LOD score for preference also associates with this scaffold. Furthermore, a non-synonymous SNP differentiating the two parental species was found in the conserved cyclic nucleotide binding domain 39 . Although unknown in Laupala , Drosophila Cngl is expressed in brain, thoracic ganglia and muscles 51 , consistent with the expectation for a causal gene for song and preference variation.…”

“…These co-localized loci explain approximately 9% and 15% of the species difference in pulse rate and pulse rate preference, respectively. We subsequently isolated and fine-mapped a song QTL on LG5 that explains an additional ~11% of the pulse rate difference of this species pair 39 . Marker association studies have predicted the existence of a preference QTL on LG5, yet its location on this linkage group remains unknown 40,41 .…”