Abstract
In the Allonemobius socius complex of crickets, reproductive isolation is primarily accomplished via postmating prezygotic barriers. We tested seven protein-coding genes expressed in the male ejaculate for patterns of evolution consistent with a putative role as postmating prezygotic isolation genes. Our recently diverged species generally lacked sequence variation. As a result, ω-based tests were only mildly successful. Some of our genes showed evidence of elevated ω values on the internal branches of gene trees. In a couple of genes, these internal branches coincided with both species branching events of the species tree, between A. fasciatus and the other two species, and between A. socius and A. sp. nov. Tex. In comparison, more successful approaches were those that took advantage of the varying degrees of lineage sorting and allele sharing among our young species. These approaches were particularly powerful within the contact zone. Among the genes we tested we found genes with genealogies that indicated relatively advanced degrees of lineage sorting across both allopatric and contact zone alleles. Within a contact zone between two members of the species complex, only a subset of genes maintained allelic segregation despite evidence of ongoing gene flow in other genes. The overlap in these analyses was arginine kinase (AK) and apolipoprotein A-1 binding protein (APBP). These genes represent two of the first examples of sperm maturation, capacitation, and motility proteins with fixed non-synonymous substitutions between species-specific alleles that may lead to postmating prezygotic isolation. Both genes express ejaculate proteins transferred to females during copulation and were previously identified through comparative proteomics. We discuss the potential function of these genes in the context of the specific postmating prezygotic isolation phenotype among our species, namely conspecific sperm precedence and the superior ability of conspecific males to induce oviposition in females.
Highlights
Not all genes contribute to reproductive isolation during speciation
We examined seven ejaculate proteins (EPs) coding genes, five of which were identified in a comparative proteome study between A. socius and A. fasciatus (Marshall et al, 2011), and two additional EP coding genes identified from unpublished EST libraries of A. socius accessory glands and testes (Marshall et al, 2011)
Using single likelihood ancestor counting (SLAC) and comparing model fits of nucleotide substitution models and codon models, for most genes (ACG69, arginine kinase (AK), APBP, serine protease inhibitor (SPI), sperm-associated antigen 6 (SPAG6)) we found no evidence of any specific sites evolving under positive or negative selection
Summary
Not all genes contribute to reproductive isolation during speciation. ‘Speciation’ (Wu, 2001; Wu & Ting, 2004; Nosil & Schluter, 2011), ‘isolation’ (Rieseberg, Church & Morjan, 2004), or ‘barrier’ (Noor & Feder, 2006) genes are expected to show very differentHow to cite this article Noh and Marshall (2016), Sorted gene genealogies and species-specific nonsynonymous substitutions point to putative postmating prezygotic isolation genes in Allonemobius crickets. Similar patterns have been observed in mice and primates (Clark & Swanson, 2005; Karn et al, 2008; Ramm et al, 2008; Turner, Chuong & Hoekstra, 2008; Dean et al, 2009). Because they enable us to isolate male reproductive protein-coding genes that can directly interact with their female counterparts, proteomic analyses of insect spermatophores have proved to be effective for narrowing prospects in the search for putative speciation genes (Andrés, Maroja & Harrison, 2008; Marshall et al, 2011; Andrés et al, 2013)
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