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

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.

Patterns of Genomic Diversity in a Fig-Associated Close Relative of Caenorhabditis elegans

“…Fig nematodes may also do this, which could generate such asymmetrical patterns on the X chromosome. A highly speculative explanation for this observation could be environmental sex determination (ESD)—in fig-associated Parasitodiplogaster and Ficophagus nematodes, sex ratios in syconia were more female-biased than those observed on fig wasps ( Van Goor et al 2022 ). Moreover, nematode sex ratios in syconia had a far lower variance than expected ( Van Goor et al 2022 ).…”

“…A highly speculative explanation for this observation could be environmental sex determination (ESD)—in fig-associated Parasitodiplogaster and Ficophagus nematodes, sex ratios in syconia were more female-biased than those observed on fig wasps ( Van Goor et al 2022 ). Moreover, nematode sex ratios in syconia had a far lower variance than expected ( Van Goor et al 2022 ). If ESD can transform X0 animals into females, ESD could promote high observed X chromosome inbreeding coefficients (as X0 females would appear to be entirely homozygous on the X chromosome), as well as lead to the kinds of demographic scenarios that can increase inbreeding coefficients on the X chromosome ( Wang 1999 ; Crow and Kimura 2009 ).…”

Fine‐scale distribution of the lungworm Halocercus delphini in the lungs of the striped dolphin, Stenella coeruleoalba: implications about migration pathways and functional significance

“…It may be that females just have a longer lifespan (for pseudaliids, see Measures, 2001). However, a female‐biased sex ratio could also be adaptive; based on theoretical grounds, it maximizes the mean number of mated females per host when the mating system is polygamous and the parasite distribution among hosts is aggregated (May & Woolhouse, 1978; Van Goor et al, 2022).…”

Effect of Ultraviolet-B Radiating Drosophila melanogaster as Host on the Quality of Trichopria drosophilae, a Pupal Parasitoid of Drosophila suzukii

“…As an important indicator of parasitoids for biological control, obtaining as many females as possible can improve the efficiency of pest control, and it is also an important guide for the mass rearing of parasitoids [ 70 , 71 , 72 , 73 ]. The sex ratio of UVB-irradiated hosts supplied with T. drosophilae increased with radiation time to a maximum of 7 h. Changing temperatures are also a key factor for the effectiveness of control when carrying out field applications of parasitoids.…”