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.
Highlights
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
Using the high posterior probability (HPP) tree set with all 109 taxa included, we calculate a mean AICc difference of –8.04 indicating that the two-rate model allowing for transition from haplodiploidy to diplodiploidy is the best fit for the data
We address the evolutionary dynamics of haplodiploidy in mites using a comparative approach
Summary
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. 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. Many authors have considered different scenarios for its evolution, and a wealth of theory has been developed on this topic (Brown 1964; Bull 1979, 1983; Borgia 1980; Sabelis and Nagelkerke 1988; Haig 1993aa,b; Goldstein 1994; Smith 2000; Normark 2004, 2006; Burt and Trivers 2006; Immler and Otto 2014) Few of these ideas have been tested in an empirical or comparative framework.
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