The evolutionary dynamics of haplodiploidy: Genome architecture and haploid viability

Abstract

Haplodiploid reproduction, in which males are haploid and females are diploid, is widespread among animals, yet we understand little about the forces responsible for its evolution. The current theory is that haplodiploidy has evolved through genetic conflicts, as it provides a transmission advantage to mothers. Male viability is thought to be a major limiting factor; diploid individuals tend to harbor many recessive lethal mutations. This theory predicts that the evolution of haplodiploidy is more likely in male heterogametic lineages with few chromosomes, as genes on the X chromosome are often expressed in a haploid environment, and the fewer the chromosome number, the greater the proportion of the total genome that is X-linked. We test this prediction with comparative phylogenetic analyses of mites, among which haplodiploidy has evolved repeatedly. We recover a negative correlation between chromosome number and haplodiploidy, find evidence that low chromosome number evolved prior to haplodiploidy, and that it is unlikely that diplodiploidy has reevolved from haplodiploid lineages of mites. These results are consistent with the predicted importance of haploid male viability.

Keywords: Acari; chromosomal evolution; haplodiploidy; reproductive strategies; sex determination.

Figure 1

Ancestral state reconstructions. (A) Posterior probability of diplodiploidy under a model in which transition from haplodiploidy (blue) to diploidy (red) is allowed. (B) Posterior probability of diplodiploidy under a model in which transition from haplodiploidy to diplodiploidy is not possible. Black boxes in (A) and (B) indicate the portion of the tree in which reconstructions differ between models. (C) Maximum‐likelihood reconstruction of diploid chromosome number. The arrow in (A) and (B) indicates the family Parasitidae that was removed for one analysis.

Figure 2

The relationship between chromosome number and ploidy across the Acari. (A) Scatterplot of all available estimates of chromosome number of haplodiploid and diplodiploid taxa for which taxonomic data were available. The black diamonds and error bars show the model prediction (posterior mean and 95% CI) of a taxonomic mixed model in MCMCglmm. (B) Scatterplot of all available estimates of chromosome number of haplodiploid and diplodiploid taxa for which phylogenetic data were available. The black diamonds and error bars show the model prediction (posterior mean and 95% CI) of a phylogenetic mixed model in MCMCglmm.