Sperm-related phenotypes implicated in both maintenance and breakdown of a natural species barrier in the house mouse

Jana Albrechtová,Jaroslav Piálek,Priscilla K Tucker,Miloš Macholán,Geir Rudolfsen,Tomáš Albrecht,Stuart J E Baird,Pavel Munclinger

doi:10.1098/rspb.2012.1802

Abstract

The house mouse hybrid zone (HMHZ) is a species barrier thought to be maintained by a balance between dispersal and natural selection against hybrids. While the HMHZ is characterized by frequency discontinuities for some sex chromosome markers, there is an unexpected large-scale regional introgression of a Y chromosome across the barrier, in defiance of Haldane's rule. Recent work suggests that a major force maintaining the species barrier acts through sperm traits. Here, we test whether the Y chromosome penetration of the species barrier acts through sperm traits by assessing sperm characteristics of wild-caught males directly in a field laboratory set up in a Y introgression region of the HMHZ, later calculating the hybrid index of each male using 1401 diagnostic single nucleotide polymorphisms (SNPs). We found that both sperm count (SC) and sperm velocity were significantly reduced across the natural spectrum of hybrids. However, SC was more than rescued in the presence of the invading Y. Our results imply an asymmetric advantage for Y chromosome introgression consistent with the observed large-scale introgression. We suggest that selection on sperm-related traits probably explains a large component of patterns observed in the natural hybrid zone, including the Y chromosome penetration.

Highlights

Most models of speciation involve periods of hybridization [1]
Such disruptions are observed when genetically divergent taxa are crossed in the laboratory: male F1s are often completely sterile or produce malformed sperm. The relevance of these phenotypes to the balance of forces in the house mouse hybrid zone (HMHZ) has been questioned for some time [25] because of the disconnect between the early-generation hybrids studied in the laboratory versus the late-generation hybrids present in nature, but recent work [15] has considerably reduced this gap by sampling hybrids from localities within the HMHZ, crossing individuals from the same or nearby localities in the laboratory, and measuring sperm traits of their progeny. It does not allow for the effects of mate choice and sperm competition on the frequency spectrum of hybrids in nature, this study provides the most direct evidence to date that hybrid dysgenesis affecting sperm count (SC) and velocity may be major effects acting to maintain the mouse species barrier, while the variability of the traits indicate that these phenotypes are under highly polygenic control [15]
The documented degree of sterility of laboratory mouse F1 males might potentially explain the narrowness of the European HMHZ, it has repeatedly been shown that F1 males are extremely rare, if not absent entirely [5,9,10,15]

Summary

Introduction

Most models of speciation involve periods of hybridization [1]. Understanding the balance of forces acting during hybridization is a great aid to understanding speciation itself [2]. We suggest that selection on sperm-related traits probably explains a large component of patterns observed in the natural hybrid zone, including the Y chromosome penetration.

Results

Conclusion