Abstract

Reproductive isolation at the gamete stage has become a focus of speciation research because of its potential to evolve rapidly between closely related species. Conspecific sperm precedence (CSP), a type of gametic isolation, has been demonstrated in a number of taxa, both marine and terrestrial, with the potential to play an important role in speciation. Free-spawning marine invertebrates are ideal subjects for the study of CSP because of a likely central role for gametic barriers in reproductive isolation. The western Atlantic Mytilus blue mussel hybrid zone, ranging from the Atlantic Canada to eastern Maine, exhibits characteristics conducive to the study of CSP. Previous studies have shown that gametic incompatibility is incomplete, variable in strength and the genotype distribution is bimodal—dominated by the parental species, with a low frequency of hybrids. We conducted gamete crossing experiments using M. trossulus and M. edulis individuals collected from natural populations during the spring spawning season in order to detect the presence or absence of CSP within this hybrid zone. We detected CSP, defined here as a reduction in heterospecific offspring from competitive fertilizations in vitro compared to that seen in non-competitive fertilizations, in five of the twelve crosses in which conspecific crosses were detectable. This is the first finding of CSP in a naturally hybridizing population of a free-spawning marine invertebrate. Our findings support earlier predictions that CSP can promote assortative fertilization in bimodal hybrid zones, further advancing their hypothesized progression towards full speciation. Despite strong CSP numerous heterospecific fertilizations remain, reinforcing the hypothesis that compatible females are a source of hybrid offspring in mixed natural spawns.

Highlights

  • Conspecific sperm precedence (CSP) is a post-mating, prezygotic reproductive barrier and is defined as a non-random increase in fertilization success of conspecific sperm when an egg is challenged with both conspecific and heterospecific sperm simultaneously [1]

  • In our work over 9 years in eastern Maine, we found that M. trossulus females spawned in response to induction much less frequently than M. edulis females, and in the present study, too few M. trossulus females spawned to provide combinations needed to study CSP in this direction

  • Our results demonstrate conspecific sperm precedence in M. edulis females in a direct comparison of non-competitive and competitive crossing experiments with M. trossulus

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Summary

Introduction

Conspecific sperm precedence (CSP) is a post-mating, prezygotic reproductive barrier and is defined as a non-random increase in fertilization success of conspecific sperm when an egg is challenged with both conspecific and heterospecific sperm simultaneously [1]. Free-spawning marine invertebrates have few, if any, mating-associated behaviors, with the exception of possible prespawning chemical cues and aggregative behaviors at spawning [9] Given this short list of candidate prespawning isolating barriers, interaction and competition between conspecific and heterospecific gametes may be crucial to reproductive isolation in mixed-species populations. Rawson et al [11] and Slaughter et al [12], studied gamete incompatibility in vitro between M. edulis and M. trossulus These studies were conducted in a non-competitive format by mixing the eggs of a single female with varying dilutions of sperm from a single male, carefully quantifying compatibility of all possible male/female combinations, and comparing the results for both intraspecific combinations with those from the two reciprocal interspecific crosses.

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