The geography of sex: sexual conflict, environmental gradients and local loss of sex in facultatively parthenogenetic animals

Abstract

Obligately asexual organisms tend to occur at higher altitudes or latitudes and occupy larger ranges than their obligately sexual relatives-a phenomenon called geographical parthenogenesis. Some facultatively parthenogenetic organisms that reproduce both sexually and asexually also exhibit spatial variation in reproductive mode. Theory suggests that sexual conflict and mate limitation can determine the relative frequency of sex in facultative parthenogens, but the effect of these dynamics on spatial distributions is unknown. Here, we use individual-based models to investigate whether these dynamics can generate local differences in the reproductive mode in a facultatively parthenogenetic metapopulation occupying an environmental gradient. We find that selection for resistance and high fecundity creates positive epistasis in virgin females between a mutant allele for parthenogenesis and alleles for resistance, resulting in female-biased sex ratios and higher resistance and coercion towards the productive 'core' of the metapopulation. However, steeper environmental gradients, which lead to lower density and less mating at the 'edge', generate female bias without promoting coercion or resistance. Our analysis shows that local adaptation of facultatively parthenogenetic populations subject to sexual conflict and productivity gradients can generate striking spatial variation suggesting new patterns for empirical investigation. These findings could also help to explain the rarity of facultative parthenogenesis in animals.This article is part of the theme issue 'Linking local adaptation with the evolution of sex differences'.

Keywords: environmental gradient; facultative parthenogenesis; geographical parthenogenesis; individual-based model; paradox of sex; sexual conflict.

Figure 1.

Spatial structure of the simulated environment, showing the eight linear habitats that decline in productivity from core to edge, and the n × n patches within each habitat. A female (back square) is shown surrounded by eight potential mates (grey squares).

Figure 2.

Life cycle of sexual (a) and mutant (b) organisms, showing the progression of life stages (squares) and the processes that occur at each stage (diamonds).

Figure 3.

Heat maps showing spatial patterns for sex ratio (a), frequency of pooled resistance alleles (b), population density (c) and frequency of pooled coercion alleles (d) in metapopulations with no initial refugia. The core population is represented by distance 0 on the bottom x-axis; distance 7 is the edge population. The top x-axis shows the relative fecundity of parthenogenesis, ɛ. The left-hand y-axis depicts m, the female fitness gradient, which controls the intensity of sexual conflict. The right-hand y-axis shows the steepness of the ecocline, κ. Values closer to 1 signify more female-biased sex ratios (a), higher frequencies of resistance alleles (b), higher densities (c), and higher frequencies of coercion alleles (d). White regions in panel (d) indicate male extinctions. Outcomes are median proportions obtained from 50 simulation runs lasting 500 generations each. (Online version in colour.)

Figure 4.

Segment graphs showing core-to-edge differences in sex ratio, frequency of pooled resistance alleles and frequency of pooled coercion alleles following relaxation of model assumptions from baseline settings for simulations with no global fecundity ecocline (κ = 0) (a), a shallow ecocline (κ = 0.4) (b) and a steep ecocline (κ = 0.7) (c). Crosses denote median ratios/frequencies for core and edge populations obtained from 50 simulation runs. Segment lengths indicate the size of core-to-edge differences. Parameters controlling sexual coevolution, costs of coercion and resistance, level of maximum productivity and refugia size were perturbed independently of each other. Baseline parameter settings are listed in electronic supplementary material, table S1. (Online version in colour.)

Figure 5.

Heat maps showing mean female fitness as a function of resistance allele number (y-axis), reproductive-mode genotype (x-axis, top row) and mating status (x-axis, bottom row). Each plot is a snapshot of female fitness at the core (a,c) and the edge (b,d) at time-step 75 (a,b) and time-step 250 (c,d) from a single simulation run. During the early stages of invasion, positive epistasis for fitness between the P allele and resistance alleles occurs at the core (a), where pP and PP genotypes are associated with a larger number of resistance alleles than the pp genotype, and where these combinations of alleles for parthenogenesis and resistance achieve higher fitness when mating is avoided. By contrast, at the edge (b), there is no association between parthenogenesis or resistance genotype and fitness. Following fixation of the P allele, females at the core carry more resistance alleles (c) than females at the edge (d) as a consequence of this past epistasis. Other parameters: small refugia, κ = 0.7, m = 1.5, ɛ = 0.9. (Online version in colour.)