Chromosome inheritance and reproductive barriers in backcrosses between two hybridizing Viviparus snail species

Abstract

Hybridization must be followed by repeated backcrossing of the subsequent hybrid generations to the parental species for gene exchange between species to occur. Due to meiotic failures, first-generation hybrids of some species produce unreduced gametes. Their progeny in backcrosses with a diploid parental species are polyploid and functionally sterile. Polyploidy of the backcross generation may therefore act as an instantaneous barrier to gene flow between hybrids and the parental species. Here we determined chromosome inheritance in backcrosses of two hybridizing freshwater caenogastropod snail species to assess whether gene introgression is inhibited in the first backcross generation. Viviparus ater and V. contectus intermate in nature and produce viable F1 hybrid progeny, although offspring sex ratio is strongly male biased. Despite the different chromosome numbers of the two parental species (V. ater, 2n = 18; V. contectus, 2n = 14), the F1 hybrids are able to reproduce. Allozyme data from natural populations are compatible with gene exchange between the two species, although there is also evidence suggesting that some alleles may be shared because of common ancestry. Our study revealed that all viable backcross progeny were homoploid as they inherited between seven and nine chromosomes from the hybrid father. The siring success of the karyotypically different hybrid sperm was skewed against one sperm karyotype depending on the non-hybrid mother in the cross. In backcross broods of V. ater females, the observed distribution of the karyotypes conformed with an assumption of random segregation of two unpaired chromosomes at meiosis in hybrid males. In contrast, when backcrossing hybrid males to V. contectus females, post-copulatory processes ultimately determined the karyotype distribution of the backcross progeny. Homoploidy of all backcross progeny together with the presence of sperm and embryos in their gonads makes gene exchange between the two parental species through hybridization possible.