Sexual morph specialisation in a trioecious nematode balances opposing selective forces

Abstract

The coexistence of different mating strategies, whereby a species can reproduce both by selfing and outcrossing, is an evolutionary enigma. Theory predicts two predominant stable mating states: outcrossing with strong inbreeding depression or selfing with weak inbreeding depression. As these two mating strategies are subject to opposing selective forces, mixed breeding systems are thought to be a rare transitory state yet can persist even after multiple speciation events. We hypothesise that if each mating strategy plays a distinctive role during some part of the species life history, opposing selective pressures could be balanced, permitting the stable co-existence of selfing and outcrossing sexual morphs. In this scenario, we would expect each morph to be specialised in their respective roles. Here we show, using behavioural, physiological and gene expression studies, that the selfing (hermaphrodite) and outcrossing (female) sexual morphs of the trioecious nematode Auanema freiburgensis have distinct adaptations optimised for their different roles during the life cycle. A. freiburgensis hermaphrodites are known to be produced under stressful conditions and are specialised for dispersal to new habitat patches. Here we show that they exhibit metabolic and intestinal changes enabling them to meet the cost of dispersal and reproduction. In contrast, A. freiburgensis females are produced in favourable conditions and facilitate rapid population growth. We found that females compensate for the lack of reproductive assurance by reallocating resources from intestinal development to mate-finding behaviour. The specialisation of each mating system for its role in the life cycle could balance opposing selective forces allowing the stable maintenance of both mating systems in A. freiburgensis.

The contribution of an X chromosome QTL to non-Mendelian inheritance and unequal chromosomal segregation inA. freiburgense

“…Here we tested two A. freiburgense inbred strains, APS7 and APS14 [19], which produced 18% or fewer sons after outcrossing (Table 1) [20].The high ratio of XX offspring confirms previous studies with other strains of the same species [13,18].…”

“…Chromosomal-level genome assembly of A. freiburgense Auanema populations consist of selfing hermaphrodites, females, and males [16,18]. Hermaphrodite development is determined intergenerationally according to maternal age in A. rhodense [22,27,28], or social cues in A. freiburgense [19,29,30] and A. melissense [31]. XO males produce predominantly X-bearing sperm [12,13], resulting in XX offspring when mating with females [16].…”

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

“…In A. freiburgensis , it has been proposed that females and hermaphrodites may play different roles in the life cycle, with each sexual morph exhibiting adaptations specific to their part, stabilizing trioecy in the population ( Adams et al, 2022 ). A. freiburgensis hermaphrodites invest resources in the expansion of the intestine, the major metabolic organ, which may enable them to meet the high energy cost of dispersal and reproduction ( Adams et al, 2022 ). In contrast, the obligate outcrossing female diverts resources from intestinal development to invest in mate-finding behavior ( Adams et al, 2022 ).…”

“…A. freiburgensis hermaphrodites invest resources in the expansion of the intestine, the major metabolic organ, which may enable them to meet the high energy cost of dispersal and reproduction ( Adams et al, 2022 ). In contrast, the obligate outcrossing female diverts resources from intestinal development to invest in mate-finding behavior ( Adams et al, 2022 ). Here we show that the sexual morphs of A. melissensis exhibit similar developmental differences.…”

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

“…In the species in which trioecy has been studied and monitored, it is noticeable that their populations are subjected to strong environmental stress in situ or under laboratory manipulation 50 – 52 . For example, some nematodes of the genus Tokorhabditis are extremophilic species that live in the Californian Mono Lake, which is characterized by being hypersaline and exhibiting high levels of arsenic 10 , 50 .…”