Abstract
Trioecy, the co-occurrence of males, females and hermaphrodites in natural populations, is a relatively common sexual system in plants, but is rare and poorly understood in animals. Previously, the marine mussel, Semimytilus algosus, has been described as a simultaneous hermaphrodite and there are reports of unisex animals in the wild. Here, we confirm trioecy in this bivalve, the first report of trioecy in the phylum Mollusca. We examined the frequencies of females, males and hermaphrodites in seven natural populations along a latitudinal gradient of ~2500 km and carried out a phylogenetic analysis with mussel species of the family Mytilidae with known sexual systems. Hermaphrodites (~95.3%), females (~3.6%), and males (~1.1%) were found in all seven populations across the species’ range in Chile. The consistent sex ratios across all populations suggest that the sexual system is stable in space. Phylogenetic analysis (mDNA) of members of the family Mytilidae indicates that this species alone has developed trioecy from dioecious ancestors. As unisex animals were the least common in the wild, it is likely that these animals, especially males, might be in the process of being lost in this species, and that trioecy might be an intermediate step towards gynodioecy or hermaphroditism. The reproductive characteristics of S. algosus make it an excellent model species for the study of the evolution of sexual systems in animals and also possibly the processes underlying sex determination in molluscs.
Highlights
One of the fundamental challenges of evolutionary biology is to understand breeding systems and to determine how and why different breeding systems exist (Darwin, 1876; Maynard Smith, 1978)
Whilst a range of different breeding systems exist amongst the Animalia, there are two common sexual systems, dioecy, in which individuals are either male or female during their reproductive lives but not both, and hermaphroditism, in which animals produce both eggs and sperm during their breeding lives
The objectives of the present work were: (1) to test our hypothesis that the mussel, S. algosus, has evolved a sexual system based on trioecy, (2) to examine the spatial stability of the sexual system across multiple independent populations along a natural latitudinal gradient of ∼ 2500 km, and (3) determine the phylogenetic position of this mussel within the broader evolutionary context of the family Mytilidae of the phylum Mollusca, that is known to exhibit dioecy
Summary
One of the fundamental challenges of evolutionary biology is to understand breeding systems and to determine how and why different breeding systems exist (Darwin, 1876; Maynard Smith, 1978). With regard to the first question, a number of different factors have been identified or proposed as being important in promoting the existence of different breeding systems, in particular in plants (Barrett, 2002; Jones et al, 2013; Petry et al, 2016; Ansaldi et al, 2018), sometimes within populations of the same species in close geographic proximity. In particular with regard to the second point, Fleming et al (1998) note that trioecy can be a stable sexual system in this cactus when bat pollinators are limited in their abundance
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