Environmental stress maintains trioecy in nematode worms

Abstract

Sex is determined by chromosomes in mammals but it can be influenced by the environment in many worms, crustaceans, and vertebrates. Despite this, there is little understanding of the relationship between ecology and the evolution of sexual systems. The nematode Auanema freiburgensis has a unique sex determination system in which individuals carrying one X chromosome develop into males while XX individuals develop into females in stress‐free environments and self‐fertile hermaphrodites in stressful environments. Theory predicts that trioecious populations with coexisting males, females, and hermaphrodites should be unstable intermediates in evolutionary transitions between mating systems. In this article, we study a mathematical model of reproductive evolution based on the unique life history and sex determination of A. freiburgensis. We develop the model in two scenarios, one where the relative production of hermaphrodites and females is entirely dependent on the environment and one based on empirical measurements of a population that displays incomplete, “leaky” environmental dependence. In the first scenario environmental conditions can push the population along an evolutionary continuum and result in the stable maintenance of multiple reproductive systems. The second “leaky” scenario results in the maintenance of three sexes for all environmental conditions. Theoretical investigations of reproductive system transitions have focused on the evolutionary costs and benefits of sex. Here, we show that the flexible sex determination system of A. freiburgensis may contribute to population‐level resilience in the microscopic nematode's patchy, ephemeral natural habitat. Our results demonstrate that life history, ecology, and environment may play defining roles in the evolution of sexual systems.

De novo Genome Assembly of Auanema melissensis, a Trioecious Free-Living Nematode

“…In laboratory cultures, XO males are in lower proportions (typically 5–15%) than XX non-males (females and hermaphrodites) ( Félix, 2004 ; Chaudhuri et al, 2011a , 2015; Shakes et al, 2011 ; Robles et al, 2021 ). The dynamics of this unusual mating system is poorly understood ( Anderson et al, 2020 ; Rupp, 2020 ). In the species described so far, Auanema rhodensis (aka Rhabditis sp.…”

The eco‐evolutionary importance of reproductive system variation in the macroalgae: Freshwater reds as a case study

“…Contrary to work that has suggested trioecy (males, females, and hermaphroditic individuals) is a transitory state (Lande & Schemske, 1985), Anderson et al. (2020) has shown that trioecy can be stable and reap the benefits of outcrossing and reproductive assurance. Yet, understanding reproductive system variation necessitates integrative ecological and genetic approaches to disentangle the forces that drive transitions in sexual system (see Table 1) and how that influences the reproductive system.…”

“…In disturbed habitats, such as those where frequent extinction and colonization events occur, monoecious individuals will have a selective advantage, as only one individual is necessary to (re-)establish the population (Baker, 1955). Contrary to work that has suggested trioecy (males, females, and hermaphroditic individuals) is a transitory state , Anderson et al (2020) has shown that trioecy can be stable and reap the benefits of outcrossing and reproductive assurance. Yet, understanding reproductive system variation necessitates integrative ecological and genetic approaches to disentangle the forces that drive transitions in sexual system (see Table 1) and how that influences the reproductive system.…”

Trioecy is maintained as a time-stable mating system in the pink sea urchin Toxopneustes roseus from the Mexican Pacific

“…The trioecic condition has been recorded so far only in some animals, such as a few nematode species and a hydra 9 , 10 , 14 , 46 – 48 . In marine invertebrates, it has been reported in one anemone under laboratory conditions and in one bivalve mollusk 15 , 16 .…”