Abstract
The lifetime monogamy hypothesis claims that the evolution of permanently unmated worker castes always requires maximal full-sibling relatedness to be established first. The long-lived diploid ambrosia beetle Austroplatypus incompertus (Schedl) is known to be highly social, but whether it has lifetime sterile castes has remained unclear. Here we show that the gallery systems of this beetle inside the heartwood of live Eucalyptus trees are always inhabited by a single core family, consisting of a lifetime-inseminated mother, permanently unmated daughter workers, and immatures that are always full siblings to each other and their adult caretakers. Overall sex ratios are even. Males always disperse and only survive as stored sperm, but female offspring either disperse to mate and found their own colony or assume unmated worker roles, probably surviving for many years without any reproductive potential because tarsal loss precludes later dispersal. A well-supported Platypodinae phylogeny has allowed us to infer that parental monogamy evolved before a lifetime-unmated worker caste emerged, confirming the prediction that monogamy and full-sibling relatedness are necessary conditions for the evolution of such workers. The initially very challenging but ultimately long-term stable nesting habitat in live trees appears to have provided the crucial benefit/cost factor for maintaining selection for permanently sterile workers after strict monogamy and lifetime sperm storage had become established in this curculionid coleopteran lineage.
Highlights
one locus showed a significant deficiency of heterozygotes compared with expected Hardy-Weinberg equilibrium
sampling regimes were employed at three locations in New South Wales
E. agglomerata trees enabled the investigation of gallery system phenology
Summary
Founding A. incompertus females excavate galleries in live Eucalyptus trees[26] that are later occupied by new generations of females, along with larvae and eggs[15]. The significant quadratic term in polynomial regression (Fig. 4b) of dispersing females on dispersing males indicates that young colonies recruiting workers for the first time release an excess of males, while old colonies contribute relatively more dispersing females This is consistent with negative frequency dependent selection maintaining an equilibrium population-wide sex ratio to which colonies contribute in a split manner depending on developmental stage. Full-sibling relatedness appears to be maintained, consistent with neither the foundress re-mating later in life nor any helping daughter becoming inseminated after having assumed sterile worker tasks These data showed that colony usurpation by a newly mated younger breeder had not occurred (see Supplementary Information). Observed relatedness values were not significantly different from a simulated distribution of relatedness values for 6,000 full-sibling dyads randomly generated from our populationwide allele frequency distributions (P =0 .61), which produced an expected nestmate relatedness of 0.497 ± 0.003 (95% CI)
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