Extraordinarily precise nematode sex ratios: adaptive responses to vanishingly rare mating opportunities.

Justin Van Goor,Adalberto Gómez,John D Nason,Edward Allen Herre

doi:10.1098/rspb.2021.1572

Justin Van Goor, Adalberto Gómez + Show 2 more

Open Access

https://doi.org/10.1098/rspb.2021.1572

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Abstract

Sex ratio theory predicts both mean sex ratio and variance under a range of population structures. Here, we compare two genera of phoretic nematodes (Parasitodiplogaster and Ficophagus spp.) associated with 12 fig pollinating wasp species in Panama. The host wasps exhibit classic local mate competition: only inseminated females disperse from natal figs, and their offspring form mating pools that consist of scores of the adult offspring contributed by one or a few foundress mothers. By contrast, in both nematode genera, only sexually undifferentiated juveniles disperse and their mating pools routinely consist of 10 or fewer adults. Across all mating pool sizes, the sex ratios observed in both nematode genera are consistently female-biased (approx. 0.34 males), but markedly less female-biased than is often observed in the host wasps (approx. 0.10 males). In further contrast with their hosts, variances in nematode sex ratios are also consistently precise (significantly less than binomial). The constraints associated with predictably small mating pools within highly subdivided populations appear to select for precise sex ratios that contribute both to the reproductive success of individual nematodes, and to the evolutionary persistence of nematode species. We suggest that some form of environmental sex determination underlies these precise sex ratios.

Highlights

Sex ratio theory provides testable, quantitative predictions of population and individual adaptations expected under a wide range of selective regimes
Parasitodiplogaster nematode infections occurred in all 12 sampled Ficus species, while Ficophagus infections occurred in nine
Of the 593 figs with detailed information on mating pool composition for Parasitodiplogaster, Ficophagus or both, 413 were pollinated by a single wasp foundress, in which case all nematodes involved in a mating pool arrived together with a single wasp

Summary

Introduction

Sex ratio theory provides testable, quantitative predictions of population and individual adaptations expected under a wide range of selective regimes. Following Darwin [1] and Düsing [2], Fisher [3] argued that natural selection within populations of species with separate sexes should favour equal parental investment in the sexes, generally resulting in a population-wide 1 : 1 (0.50 males) sex ratio [4]. Darwin knew that many organisms do not exhibit a 1 : 1 sex ratio, famously stating ‘the whole problem is so intricate that it is safer to leave its solution for the future’ [5]. Many species are characterized by subdivided population structures, with male and female adults typically mating in isolated patches. Mated females disperse from these patches and typically one or a few foundresses contribute offspring to subsequent mating pools [6,7,8]

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