Multivariate Models of Animal Sex: Breaking Binaries Leads to a Better Understanding of Ecology and Evolution

Abstract

‘Sex’ is often used to describe a suite of phenotypic and genotypic traits of an organism related to reproduction. However, these traits – gamete type, chromosomal inheritance, physiology, morphology, behavior, etc. – are not necessarily coupled, and the rhetorical collapse of variation into a single term elides much of the complexity inherent in sexual phenotypes. We argue that consideration of ‘sex’ as a constructed category operating at multiple biological levels opens up new avenues for inquiry in our study of biological variation. We apply this framework to three case studies that illustrate the diversity of sex variation, from decoupling sexual phenotypes to the evolutionary and ecological consequences of intrasexual polymorphisms. We argue that instead of assuming binary sex in these systems, some may be better categorized as multivariate and nonbinary. Finally, we conduct a meta-analysis of terms used to describe diversity in sexual phenotypes in the scientific literature to highlight how a multivariate model of sex can clarify, rather than cloud, studies of sexual diversity within and across species. We argue that such an expanded framework of ‘sex’ better equips us to understand evolutionary processes, and that as biologists it is incumbent upon us to push back against misunderstandings of the biology of sexual phenotypes that enact harm on marginalized communities.

Training in the implementation of sex and gender research policies: an evaluation of publicly available online courses

“…The time is also ripe for other entities, beyond funding agencies, to develop resources that fill current gaps. Here, we outline four areas that have recently increased tremendously in their visibility and in which researchers have expressed clear interest [ 16 – 20 , 29 , 30 ]: (1) The precise and contextualized operationalization of sex; (2) The risks inherent in a “two sizes fit all” approach to sex-based research and clinical applications; (3) The entanglement of sex and gender; and (4) Attention to rigorous analytical approaches to sex-based data. We outline each of these below, in hopes that future course offerings, both new and revised, can incorporate these important topics.…”

Sex and Biology: Broader Impacts Beyond the Binary

“…The models that we are using to come up with questions about animal biology are thoroughly rooted in our cultural assumptions ( McLaughlin et al 2023 ). As AEK noted in our roundtable discussion, “Cultural norms can be so pervasive that it’s almost as if they are ‘common sense,’ so it is hard for people who see them everywhere they look not to project them onto the biology that they’re studying.” Furthering this point, JFM added “When we are looking at systems like sexual selection with birds or lizards, and we are coming from a cultural background of ‘sex is binary,’ we’re asking questions like ‘why do we have different types of males that do different things’ or ‘why are these sex roles reversed between male and female.’ These are inherently rooted in the fact that we have a culture that looks at this as a binary, but birds and lizards don’t care!”…”

“…Accompanying this roundtable summary, another article from this symposium surveys several terms in the literature that impose a binary framework onto sexual phenotypes ( McLaughlin et al 2023 ). These terms change in prevalence across time and among different taxa.…”

Yeast sexes: mating types do not determine the sexes in Metschnikowia species

“…As always, clear definitions are key to fruitful discussion. Whether biological sexes are strictly binary as opposed to part of a spectrum is currently the object of considerable debate in some circles (Goymann et al 2023 , McLaughlin et al 2023 ). The controversy is often fuelled by ambiguous terminology, where one fails to parse out secondary from primary sexual characteristics or to distinguish biological sexes from socially constructed genders.…”