Transitions in sex determination mechanisms through parental antagonism

Parental antagonism (PA) occurs when the fitness effects of a gene depend on the parent from which it is inherited. Such genes may become enriched on sex chromosomes, due to their biased inheritance patterns. Although various sex determination (SD) genes exhibit parent-of-origin effects themselves, and between-parent conflict over offspring sex may affect SD, PA itself has not been considered as a driver of SD transitions. Here, I present a model to investigate the scope for transitions in SD mechanisms through PA. My model assumes an ancestral SD locus linked to a PA gene, as well as an autosomal PA gene in whose vicinity a novel SD gene arises. Transitions between functionally-homologous genes are found to depend on the fitness effects of both PA genes and their linkage to nearby SD genes. Transitions between male and female heterogamety by the invasion of a dominant SD gene are however nearly unconstrained. This also allows for back-and-forth dynamics where the ancestral SD and novel SD genes constantly evolve to be dominant over each other. These results further underline the malleability of SD mechanisms, and the need to consider parent-of-origin effects in driving transitions in SD, through proximate and/or ultimate means

Adaptation in the face of internal conflict:The paradox of the organism revisited

The paradox of the organism refers to the observation that organisms appear to function as coherent purposeful entities, despite the potential for within-organismal components like selfish genetic elements and cancer cells to erode them from within. While it is commonly accepted that organisms may pursue fitness maximisation and can be thought to hold particular agendas, there is a growing recognition that genes and cells do so as well. This can lead to evolutionary conflicts between an organism and the parts that reside within it. Here, we revisit the paradox of the organism. We first outline its conception and relationship to debates about adaptation in evolutionary biology. Second, we review the ways selfish elements may exploit organisms, and the extent to which this threatens organismal integrity. To this end, we introduce a novel classification scheme that distinguishes between selfish elements that seek to distort transmission versus those that seek to distort phenotypic traits. Our classification scheme also highlights how some selfish elements elude a multi-level selection decomposition using the Price equation. Third, we discuss how the organism can retain its status as the primary fitness-maximising agent in the face of selfish elements. The success of selfish elements is often constrained by their strategy and further limited by a combination of fitness alignment and enforcement mechanisms controlled by the organism. Finally, we argue for the need for quantitative measures of both internal conflicts and organismality

Epistatic interactions between sex chromosomes and autosomes can affect the stability of sex determination systems

Sex determination (SD) is an essential and ancient developmental process, but the genetic systems that regulate this process are surprisingly variable. Why SD mechanisms vary so much is a longstanding question in evolutionary biology. SD genes are generally located on sex chromosomes which also carry genes that interact epistatically with autosomes to affect fitness. How this affects the evolutionary stability of SD mechanisms is still unknown. Here, we explore how epistatic interactions between a sexually antagonistic (SA) non‐SD gene, located on either an ancestral or novel sex chromosome, and an autosomal gene affect the conditions under which an evolutionary transition to a new SD system occurs. We find that when the SD gene is linked to an ancestral sex‐chromosomal gene which engages in epistatic interactions, epistasis enhances the stability of the sex chromosomes so that they are retained under conditions where transitions would otherwise occur. This occurs both when weaker fitness effects are associated with the ancestral sex chromosome pair or stronger fitness effects associated with a newly evolved SD gene. However, the probability that novel SD genes spread is unaffected if they arise near genes involved in epistasis. This discrepancy occurs because, on autosomes, SA allele frequencies are typically lower than on sex chromosomes. In our model, increased frequencies of these alleles contribute to a higher frequency of epistasis which may therefore more readily occur on sex chromosomes. Because sex chromosome–autosome interactions are abundant and can take several forms, they may play a large role in maintaining sex chromosomes

Divergent evolution of genetic sex determination mechanisms along environmental gradients

Sex determination (SD) is a crucial developmental process, but its molecular underpinnings are very diverse, both between and within species. SD mechanisms have traditionally been categorized as either genetic (GSD) or environmental (ESD), depending on the type of cue that triggers sexual differentiation. However, mixed systems, with both genetic and environmental components, are more prevalent than previously thought. Here, we show theoretically that environmental effects on expression levels of genes within SD regulatory mechanisms can easily trigger within-species evolutionary divergence of SD mechanisms. This may lead to the stable coexistence of multiple SD mechanisms and to spatial variation in the occurrence of different SD mechanisms along environmental gradients. We applied the model to the SD system of the housefly, a global species with world-wide latitudinal clines in the frequencies of different SD systems, and found that it correctly predicted these clines if specific genes in the housefly SD system were assumed to have temperature-dependent expression levels. We conclude that environmental sensitivity of gene regulatory networks may play an important role in diversification of SD mechanisms

Adult sex ratios affect mating behaviour in the common housefly <i>Musca domestica</i> L. (Diptera; Muscidae)

Adult sex ratio determines the level of mate availability and intrasexual competition for each sex. Sex ratio biases have been proposed to enhance the productivity of animal rearing procedures. However, behaviour may change in response to sex ratio manipulations that may counteract potential benefits. We investigated how sex ratios affected mating behaviour of the housefly Musca domestica, a species used in the animal feed industry. We hypothesized a reduced courtship effort and mating latency and increased ejaculate allocation (copulation duration) under male-biased sex ratios, whereas female-biased sex ratios would lead to the opposite effects. However, courtship effort was reduced in female-biased groups, implying reduced male harassment. Mating latency was lower and copulation lasted longer in female-biased groups, which may reduce reproduction time and increase female fecundity and lifespan. Our results indicate that in houseflies, female-biased sex ratios cause behavioural changes in both sexes that could positively contribute to reproductive output