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.

Keywords: Ficophagus; Ficus; Parasitodiplogaster; environmental sex determination; sex allocation; sex ratio variance.

Figure 1.

Reproductive cycles of fig from receptive A-phase to ripe E-phase with the corresponding arrival, pollination, oviposition and death of pollinator wasps, and the development, mating and dispersal of their female offspring (during C- and D-phases). The nematodes portrayed in the photographs are Parasitodiplogaster spp. Individuals of this genus consume wasp host tissues. Nematodes of the genus Ficophagus share the same essential reproductive life cycle, dispersing their natal fig as sexually undifferentiated juvenile nematodes. Similarly, they reach sexual maturity as either males or females when they are carried to a receptive fig. However, in contrast to Parasitodiplogaster, Ficophagus consume fig tissue. See electronic supplementary material, table S1 for a summary of similarities and differences between the life histories of the pollinator wasps and the two associated nematode genera. (Online version in colour.)

Figure 2.

Relative frequencies of mating pool sizes of Parasitodiplogaster and Ficophagus nematodes found within single foundress figs are nearly identical (384 and 93 mating pools, respectively). Data were collected and pooled from 12 Panamanian Ficus species, with a mean nematode infection load of 6.21 (Parasitodiplogaster) and 6.45 (Ficophagus) per individual wasp host.

Figure 3.

Comparison of the observed (solid line) and expected binomial variance (hatched lines) in the sex ratio for Parasitodiplogaster (a) and Ficophagus (b) mating pools from single foundress figs. The simulated expectations assume binomial sampling given the actual number of mating pools sampled and equal sex ratios (p_m = 0.5) or average sex ratios per genus from single foundress figs (Parasitodiplogaster: p_m = 0.315; Ficophagus: p_m = 0.353). Observed sample sizes per mating pool size are indicated at the top of (a) and (b), followed by the significance of the difference between observed and simulated sex ratios assuming p_m = 0.5 and the genus average p_m. ^*, ^**, and ^*** indicate p ≤ 0.001, p ≤ 0.01 and p ≤ 0.05, respectively. • indicates marginal significance (p = 0.1–0.05). The observed variance is consistently less than binomial expectations.

Figure 4.

The observed frequency of the near-mean sex ratio (closest local sex ratio combination to the overall mean) male–female combination (solid lines, with closed circles; see electronic supplementary material, table S3) for mating pools sampled from single foundress figs of Parasitodiplogaster (a) and Ficophagus (b). This frequency is nearly always greater than simulated expectations assuming binomial variance given the mating pool size, number of males in the near-mean sex ratio combination and either equal sex ratios (open squares; p_m = 0.5) or average sex ratios per genus (open diamonds; Parasitodiplogaster: p_m = 0.315; Ficophagus: p_m = 0.353). Observed sample sizes per mating pool size are indicated at the top of each panel followed by significance of the difference between observed and simulated near-mean sex ratio combination frequencies for either p_m = 0.5 or the genus average p_m. ^*, ^**, and ^*** indicate p ≤ 0.001, p ≤ 0.01 and p ≤ 0.05, respectively. • indicates marginal significance (p = 0.1–0.05).

Figure 5.

The three most frequently observed mating pool sex ratios (proportion of males; blue, red and green respectively) for mating pools ranging from 1 to 10 individuals in single foundress figs of Parasitodiplogaster (a) and Ficophagus (b). Accounting for the discretizing effect of small mating pool sizes on ratios, the most common sex ratios are observed to be those that are the closest possible to the mean sex ratio for all mating pool sizes greater than one. The size of the circle surrounding each datapoint indicates the proportion of data observed for a given mating pool size. Sample sizes are given in parentheses beneath each mating pool size. (Online version in colour.)