Patterns of transcriptome divergence in the male accessory gland of two closely related species of field crickets

Abstract

One of the central questions in evolutionary genetics is how much of the genome is involved in the early stages of divergence between populations, causing them to be reproductively isolated. In this article, we investigate genomic differentiation in a pair of closely related field crickets (Gryllus firmus and G. pennsylvanicus). These two species are the result of allopatric divergence and now interact along an extensive hybrid zone in eastern North America. Genes encoding seminal fluid proteins (SFPs) are often divergent between species, and it has been hypothesized that these proteins may play a key role in the origin and maintenance of reproductive isolation between diverging lineages. Hence, we chose to scan the accessory gland transcriptome to enable direct comparisons of differentiation for genes known to encode SFPs with differentiation in a much larger set of genes expressed in the same tissue. We have characterized differences in allele frequency between two populations for >6000 SNPs and >26,000 contigs. About 10% of all SNPs showed nearly fixed differences between the two species. Genes encoding SFPs did not have significantly elevated numbers of fixed SNPs per contig, nor did they seem to show larger differences than expected in their average allele frequencies. The distribution of allele frequency differences across the transcriptome is distinctly bimodal, but the relatively high proportion of fixed SNPs does not necessarily imply "ancient" divergence between these two lineages. Further studies of linkage disequilibrium and introgression across the hybrid zone are needed to direct our attention to those genome regions that are important for reproductive isolation.

Figure 1

(A) Frequency distribution of the interspecific differentiation index (D) for each of the 9731 predicted SNPs in G. firmus and G. pennsylvanicus. For any given SNP, D represents allele frequency differences between the two species (see Materials and Methods). (B) Frequency distribution of the number of highly differentiated SNPs (D ≥ 0.98) per contig.

Figure 2

Ranked distribution of the mean interspecific differentiation index ($\stackrel{-}{D}$) between G. firmus and G. pennsylvanicus for each of the 1157 contigs that showed high coverage (≥20×) and at least three SNPs (see Materials and Methods). Lightly shaded vertical lines represent the standard error.

Figure 3

Correlation between polymorphism within species (π) and divergence between G. firmus and G. pennsylvanicus.

Figure 4

DNA gene genealogies for a subset of 10 highly differentiated contigs and two seminal fluid protein genes (AG-0005F and AG-0334P). G. firmus is represented by open circles and G. pennsylvanicus by solid circles. Size of symbols is proportional to the frequency of the haplotype. Numbers on the branches represent bootstrap support values >75%.