Sexually but not parthenogenetically produced females benefit from mating in a stick insect

Abstract

1. In facultatively parthenogenetic populations, the prevalence of sexual reproduction depends on whether females mate and therefore produce sons and daughters or avoid mating and produce daughters only.2. The relative advantage of mating in such species may depend on a female's own reproductive origin (i.e. development from a fertilised or unfertilised egg) if parthenogenesis reduces heterozygosity similar to sexual inbreeding, or if it inhibits mating, sperm storage or fertilisation. But effects of reproductive origin on development and performance are poorly understood.3. Using the facultatively parthenogenetic stick insect, Extatosoma tiaratum, we quantified morphology, mating probability, and reproductive success in mated versus unmated females of sexual versus automictic (parthenogenetic) origin. 4. We found strong evidence that increased homozygosity negatively impacted some traits in parthenogenetically produced females: compared to sexually produced females, parthenogenetically produced females were smaller and more prone to deformities in vestigial wings, but not more prone to fluctuating asymmetry in their legs. 5. Parthenogenetically produced females received fewer mating attempts and avoided mating more often than sexually produced females. Yet, contrary to the expectation that sex should rescue parthenogenetic lineages from the detrimental effects of increased homozygosity, parthenogenetically produced females gained no net reproductive benefit from mating, suggesting that physiological constraints limit fitness returns of sexual reproduction for these females. 6. Our findings indicate that advantages of mating in this species depend on female reproductive origin. These results could help to explain spatial distributions of sex in facultatively parthenogenetic animals and evolutionary transitions to obligate asexuality.

Genetic and phenotypic consequences of local transitions between sexual and parthenogenetic reproduction in the wild

“…First, if females disperse more than males, they could travel further from the mixed-sex sites and establish all-female sites that could avoid male invasion for many generations. All-female sites could persist once established if parthenogenetically produced females exhibit reduced propensity of females to mate, and reduced benefits of mating, as reported for the related phasmid Extatosoma tiaratum (Burke & Bonduriansky, 2022). However, this explanation seems implausible because M. batesii adults of both sexes of this species disperse similar distances (Boldbaatar, 2022).…”

“…All-female sites could persist once established if parthenogenetically produced females exhibit reduced propensity of females to mate, and reduced benefits of mating, as reported for Extatosoma tiaratum (Burke & Bonduriansky, 2022). However, this explanation seems implausible because M. batesii adults of both sexes of this species disperse similar distances (Boldbaatar, 2022).…”

“…The apparent differences in heterozygosity levels between the reproductive modes could explain the higher rates of wing deformities in all-female sites. Parthenogenetically produced Extatosoma tiaratum females exhibit higher rates of wing deformities than do sexually produced females (Burke & Bonduriansky 2022). Likewise, multiple homozygous loss of function mutations cause wing defects in Drosophila (Terriente-Felix, López-Varea & de Celis, 2010; George et.…”

Does ecology shape geographical parthenogenesis? Evidence from the facultatively parthenogenetic stick insectMegacrania batesii

“…These results suggest that habitat-related factors, such as host plant morphology and chemistry, may not be the key determinants of sexual or parthenogenetic reproduction in these populations. Instead, this geographical pattern may have resulted primarily from sexual conflict (Burke and Bonduriansky 2018, 2019, 2022; Wilner et al in prep), from stochastic processes such as random dispersal events or male extinction in some mixed-sex populations (see Miller et al 2024), or from some combination of these factors.…”

Male contributions to female-male mutualism overcome the twofold cost of sex

“…There, negative frequency dependence (i.e., an increase in females favouring males) could work, and thus, Kawatsu's 19 conclusion that harmful males prevent the invasion of thelytoky would be valid. However, although there are some examples in insects [41][42][43][44] , facultative parthenogenesis is extremely rare and difficult to generalise.…”