Social parasitism in insects has raised major questions in evolutionary biology, firstly in terms of adaptations that parasites use to circumvent host defenses and, secondly, in terms of whether social parasites have arisen via allopatric or sympatric speciation. Here, we raise a third and major evolutionary issue: a priori considerations suggest that social parasites have much smaller effective population sizes (N e ) than their hosts, and should therefore have much slower rates of evolution than their hosts. The evolutionary arms race should therefore be weighted in favor of host species, raising the question of how social parasites have been able to persist over evolutionary time? Very few studies, however, have actually estimated the relative sizes of N e for social insects and their social parasites, and therefore the dimensions of unequal host-parasite evolutionary rates are unknown. Here, we use extensive samples of allodapine bee host species and their inquilines from two localities over multiple years to gage their relative N e s. We show that inquiline species have N e s that are about an order of magnitude lower than their hosts, so explaining the evolutionary persistence of social parasitism poses a major puzzle for evolutionary biology. We propose several hypotheses that may be able to address this puzzle and discuss how they could be evaluated.
The period of the Last Glacial Maximum (LGM) is characterised by severe cooling and extreme aridity in Australia. Australian temperate‐adapted bees experienced entirely new conditions over the LGM; however, few studies focused on the response of these key pollinators and their dependent plants to the LGM in Australia. In this study, we investigated the impact of the LGM climatic conditions on the population histories of the Australian temperate exoneurine bees regarded as critical native pollinators in the continent. To address this issue, we first identified the bee species using a combination of morphological and molecular approaches including phylogenetic and species delimitation methods. The analyses revealed three exoneurine genera, including Brevineura, Exoneura and Inquilina. Our estimated divergence time between Exoneura and Inquilina was close to that of previous phylogenetic studies of the exoneurine bees, which used different dating methods. The haplotype network analyses indicated the geographical structuring of the haplotypes within Exonuera and Inquilina species. We then utilised Bayesian skyline analyses to reconstruct demographic histories of the genus Exoneura for which sufficient haplotype diversity was found. The results showed that the population size of Exoneura species remained unchanged over the LGM or even increased shortly before it. The wide geographical distribution of the exoneurine species in Australia and earlier development of genetic and physiological adaptations are discussed as possibilities that enabled the species to maintain their population sizes over the LGM.
Adaptive evolutionary theory argues that organisms with larger effective
population size (Ne) should have higher rates of adaptive evolution and
therefore greater capacity to win evolutionary arm races. However, in
some certain cases species with much smaller Ne may be able to survive
beside their opponents for an extensive evolutionary time. Neutral
theory predicts that accelerated rates of molecular evolution in
organisms with exceedingly small Ne is due to the effects of genetic
drift and fixation of slightly deleterious mutations. We test this
prediction in two obligate social parasite species and their respective
host species from the bee tribe Allodapini. The parasites (genus
Inquilina) have been locked into a tight coevolutionary arm races with
their exclusive hosts (genus Exoneura) for ~15 million
years, even though Inquilina exhibit Ne that are an order of magnitude
smaller than their host. In this study, we compared rates of molecular
evolution between host and parasite using nonsynonymous to synonymous
substitution rate ratios (dN/dS) of eleven mitochondrial protein coding
genes sequenced from transcriptomes. Tests of selection on mitochondrial
genes indicated no significant differences between host and parasite
dN/dS, with evidence for purifying selection acting on all mitochondrial
genes of host and parasite species. Several potential factors which
could weaken the inverse relationship between Ne and rate of molecular
evolution are discussed.
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