A simpler explanation for the sociality-haplodiploidy connection?

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If you’ve been following the kin selection debate- where happy, well-adjusted biologists transform into livid, spittle-flecked orcs when arguing the importance of genetic relatedness in promoting social evolution- you’ll know the curious story of how haplodiploidy fell from being a pillar of evidence for kin selection to a sideshow curiosity.

Most social insects have a genetic system where males bear a single copy of each chromosome (haploid) while females have two copies (diploid). This arrangement has odd consequences for how family members inherit genes. Especially, sisters in haplodiploid species share more alleles with each other than they would with their own offspring. They are half-way to being clones, and early proponents of genetic models of social behavior took this tight association of haplodiploidy with colonies of ants, bees, and wasps as evidence that relatedness is indeed important for sociality. Kin selection.

Yet in recent years most biologists have downplayed the haplodiploid connection, citing messiness of the real world. Many social species like termites aren’t haplodiploid, and many haplodiploid species mate so frequently as to destroy the tidy structure of the simple relatedness models. Kin selection wasn’t dead, but proponents moved to different models. Meanwhile, group selectionists took the fall of the haplodiploidy hypothesis as a sign of weakness in their opponents, and haplodiploidy is now considered as either an irrelevant distraction or as a red herring of failure.

The dismissal of haplodiploidy has always bothered me. Regardless of whose math is more correct, the basic observation remains that the most eusocial of insects are haplodiploid. Surely this can’t just be coincidence.

A new model by Gardner & Ross in American Naturalist implies we might have been overthinking the connection.

Abstract: Hamilton’s “haplodiploidy hypothesis” holds that inflated sororal relatedness has promoted altruistic sib rearing in haplodiploids, potentially explaining their apparent predisposition to eusociality. Here, we suggest that haplodiploidy may instead promote eusociality simply by facilitating sex-ratio adjustment. Specifically, haplodiploidy may enable sex-ratio bias toward the more helpful sex, owing to “local resource enhancement,” and such sex-ratio bias may promote the evolution of helping by individuals of that sex, owing to the “rarer-sex effect.” This could explain why haplodiploidy appears to have been important for eusociality in taxa with only female helpers, such as ants, wasps, and bees, but not in taxa with both male and female helpers, such as termites.

Haplodiploidy has all sorts of complex downstream consequences for relatedness, but it also confers a simple upstream advantage. Haplodiploidy allows mothers to choose whether to lay male or female eggs. Fertilize the egg? Female. Don’t fertilize? Male. If your helpers are all one sex, being able to choose offspring affinity is efficient.

This observation alone is not a novel insight, but Gardner & Ross are the first to provide a coherent mathematical structure showing how haplodiploidy might rise to prominence in social species with single-sex workers.


source: Gardner A, Ross L (2013) Haplodiploidy, Sex-Ratio Adjustment, and Eusociality. The American Naturalist. http://www.jstor.org/stable/10.1086/669147

3 thoughts on “A simpler explanation for the sociality-haplodiploidy connection?”

  1. I like it and except for the ‘good of the species’ aspect of the Wells et al. quote it seems both logically sound and simpler than relatedness (and doesn’t prevent relatedness from contributing to the development of eusociality nor any of the recent complications that have been discovered from being interesting).

    It also would seem to be a simple explanation for the prevalence of haplodiploidy in mites that colonize patchy resource and for subsocial spider mites that lead a fugitive existence (running from dying hosts and aggregating predators) where the adult female is the dispersing (or migrating if you prefer) stage. Daughters will always be more likely to carry on the mother’s lineage since they disperse and males do not. Although LMC does seem to be well supported in the few studies I’ve seen, I don’t think this would falsify dispersal being a primary impetus for the evolution of haplodiploidy and female-biased sex ratios (at least 6 independent evolutions in the mites).

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