Testing concepts on the population genetics of wild bees: Low genetic diversity and high frequencies of diploid males
A fundamental property of a population is its effective size, Ne, which determines its speed and mode of evolutionary change. Conservation genetics aims to maintain or enhance standing genetic diversity as a metric of genetic ‘health’. Wild bee pollinator populations – like other Hymenoptera – are haplodiploid (females are diploid, males are haploid) and are therefore expected to exhibit an Ne of ¾ that of equivalent diplodiploid populations. Because heterozygosity (He) is directly proportional to Ne, empirical estimates of He have been used to test whether wild bees (and Hymenoptera in general) exhibit low Ne. Allozyme-based studies have been inconclusive in supporting this hypothesis.
In addition to being haplodiploid, wild bees possess a mechanism of sex determination based on heterozygosity at the sex determining (CSD) locus; individuals heterozygous at CSD are female whereas individuals diploid but homozygous at CSD develop into more or less sterile ‘diploid males’. Theory predicts that small populations of haplopiploids may produce high frequencies of diploid males that exert a cost to the population in decreasing Ne and further decreasing genetic diversity at the CSD locus, exacerbating their impact on the genetic health of populations. Allozyme-based studies of orchid bees have been equivocal in supporting this hypothesis.
We explore the predicted relationship between He and haplodiploidy using published microsatellite DNA datasets from 290 studies across major holometabolous insect orders. Results suggest that wild bees do indeed exhibit a reduction in genetic diversity equivalent to that expected by haplodiploidy. More marked still is the reduction of eusocial species over solitary species, suggesting that eusocial wild bees might be particularly threatened by poor genetic health.
We review own and others’ empirical studies using microsatellite DNA markers of these important Neotropical wild bee pollinators. For the majority of species that have been studied to date, mainland populations show little effect of inbreeding, as measured by diploid male production. Oceanic isolation is however associated with a loss of overall genetic diversity at neutral loci, yet only a marginal increase in the frequency of diploid males. Strong balancing selection at the CSD locus may counteract effects of drift in these and other bee pollinators such that populations may rarely enter a diploid male extinction vortex. Yet habitat isolation may have a profound effect on genetic diversity at neutral loci and lead to loss of adaptive potential and genetic health in many wild bee species.