The mate recognition protein gene mediates reproductive isolation and speciation in the Brachionus plicatilis cryptic species complex

Kristin E Gribble,David B Mark Welch

doi:10.1186/1471-2148-12-134

Abstract

BackgroundChemically mediated prezygotic barriers to reproduction likely play an important role in speciation. In facultatively sexual monogonont rotifers from the Brachionus plicatilis cryptic species complex, mate recognition of females by males is mediated by the Mate Recognition Protein (MRP), a globular glycoprotein on the surface of females, encoded by the mmr-b gene family. In this study, we sequenced mmr-b copies from 27 isolates representing 11 phylotypes of the B. plicatilis species complex, examined the mode of evolution and selection of mmr-b, and determined the relationship between mmr-b genetic distance and mate recognition among isolates.ResultsIsolates of the B. plicatilis species complex have 1–4 copies of mmr-b, each composed of 2–9 nearly identical tandem repeats. The repeats within a gene copy are generally more similar than are gene copies among phylotypes, suggesting concerted evolution. Compared to housekeeping genes from the same isolates, mmr-b has accumulated only half as many synonymous differences but twice as many non-synonymous differences. Most of the amino acid differences between repeats appear to occur on the outer face of the protein, and these often result in changes in predicted patterns of phosphorylation. However, we found no evidence of positive selection driving these differences. Isolates with the most divergent copies were unable to mate with other isolates and rarely self-crossed. Overall the degree of mate recognition was significantly correlated with the genetic distance of mmr-b.ConclusionsDiscrimination of compatible mates in the B. plicatilis species complex is determined by proteins encoded by closely related copies of a single gene, mmr-b. While concerted evolution of the tandem repeats in mmr-b may function to maintain identity, it can also lead to the rapid spread of a mutation through all copies in the genome and thus to reproductive isolation. The mmr-b gene is evolving rapidly, and novel alleles may be maintained and increase in frequency via asexual reproduction. Our analyses indicate that mate recognition, controlled by MMR-B, may drive reproductive isolation and allow saltational sympatric speciation within the B. plicatilis cryptic species complex, and that this process may be largely neutral.

Highlights

Mediated prezygotic barriers to reproduction likely play an important role in speciation
Attributing speciation directly to prezygotic reproductive isolation due to the evolution of mmr-b is supported by several lines of evidence in this study: mmr-b has a significantly higher nonsynonymous:synonymous nucleotide substitution ratio than other classes of genes, suggesting divergence resulting from sexual selection around the time of speciation; B. plicatilis is a speciesrich group, as is expected in clades where sexual selection leads to speciation; there is partial premating isolation between populations of the same species; the complex is composed of closely related species that differ markedly in mating signals and preferences but that vary little in morphology or other traits; and there is asymmetry in mate preferences between males and females of different populations [6,41,42]
These finding suggest a model for mate recognition in the B. plicatilis species complex: A relatively simple set of extracellular globular coiled proteins encoded by mmr-b genes expose a variety of phosphorylated and glycosylated residues that serve as ligands to a receptor on the surface of males used to trigger copulation

Summary

Introduction

Mediated prezygotic barriers to reproduction likely play an important role in speciation. Pheromone-based mate recognition has become a focus in the study of prezygotic isolation due to the apparent high specificity in signaling, the vast diversity of signaling systems between species, its independence from environmental differences, and the direct effect of chemical cues in preventing matings between divergent types [6,7]. The evolution of chemically mediated prezygotic barriers to reproduction may play an important role in speciation. The correlation between cue diversity, evolution, and mating cannot be made directly due to the difficulty in characterizing the mating cue, identifying the gene(s) giving rise to the (often extremely complex) chemical signal, and conducting mate recognition studies in the same populations

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