Albertson, R. C. | bioRxiv Science

bioRxiv2021

Polygenic sex determination produces modular sex polymorphism in an African cichlid fish

For many vertebrates, a single genetic locus initiates a cascade of developmental sex differences in the gonad and throughout the organism, resulting in adults with two, phenotypically distinct sexes. Species with polygenic sex determination (PSD) have multiple interacting sex determination alleles segregating within a single species, allowing for more than two genotypic sexes, and scenarios where sex genotype at a given locus can be decoupled from gonadal sex. Here we investigate the effects of PSD on secondary sexual characteristics in the cichlid fish Metriaclima mbenjii, where one female (W) and one male (Y) sex determination allele interact to produce siblings with four possible sex classes: ZZXX females, ZWXX females, ZWXY females, and ZZXY males. We find that PSD in M. mbenjii produces an interplay of sex-linkage and sex-limitation resulting in modular variation in morphological and behavioral traits. Further, the evolution or introgression of a novel sex determiner creates additional axes of phenotypic variation for varied traits, including genital morphology, craniofacial morphology, gastrointestinal morphology, and home tank behaviors. In contrast to single-locus sex determination, which broadly results in sexual dimorphism, polygenic sex determination can induce higher-order sexual polymorphism. The modularity of secondary sexual characteristics produced by PSD provides novel context for understanding the evolutionary causes and consequences of maintenance, gain, or loss of sex determination alleles in populations. Significance StatementSex differences in traits can occur when those traits are modified by genetic factors inherited on sex chromosomes. We investigated how sex differences emerge in a species with more than one set of sex chromosomes, measuring a variety of morphological, physiological, and behavioral traits. Rather than exhibiting sexual dimorphism associated with primary sex, the species has higher-order sexual polymorphism in secondary sexual characteristics, or more than two phenotypic sexes. Variation in secondary sexual characteristics is modular, involving the interplay of sex-linked and sex-limited traits. Our findings provide novel implications for how sex determination systems and whole-organism fitness traits co-evolve, including that significant creation or loss of variation in diverse traits can occur during transitions among sex chromosome systems.

evolutionary biology↗

bioRxiv2020

Diversity in rest-activity patterns among Lake Malawi cichlid fishessuggests novel axis of habitat partitioning

Animals display remarkable diversity in rest and activity patterns that are regulated by endogenous foraging strategies, social behaviors, and predator avoidance. Alteration in the circadian timing of activity or the duration of rest-wake cycles provide a central mechanism for animals to exploit novel niches. The diversity of the 3000+ cichlid species throughout the world provides a unique opportunity to examine variation in locomotor activity and rest. Lake Malawi alone is home to over 500 species of cichlids that display divergent behaviors and inhabit well-defined niches throughout the lake. These species are presumed to be diurnal, though this has never been tested systematically. Here, we measure locomotor activity across the circadian cycle in 12 cichlid species from divergent lineages and distinct habitats. We document surprising variability in the circadian time of locomotor activity and the duration of rest. In particular, we identify a single species, Tropheops sp. "red cheek" that is nocturnal. Nocturnal behavior was maintained when fish were provided shelter, but not under constant darkness, suggesting it results from acute response to light rather than an endogenous circadian rhythm. Finally, we show that nocturnality is associated with increased eye size, suggesting a link between visual processing and nighttime activity. Together, these findings identify diversity of locomotor behavior in Lake Malawi cichlids and provide a system for investigating the molecular and neural basis underlying the evolution of nocturnal activity.

evolutionary biology↗