The maintenance of mitochondrial genetic variation by negative frequency-dependent selection.

Mitochondrial genes generally show high levels of standing genetic variation, which is puzzling given the accumulating evidence for phenotypic effects of mitochondrial genetic variation. Negative frequency-dependent selection, where the relative fitness of a genotype is inversely related to its frequency in a population, provides a potent and potentially general process that can maintain mitochondrial polymorphism. We assessed the change in mitochondrial haplotype frequencies over 10 generations of experimental evolution in 180 seed beetle populations in the laboratory, where haplotypes competed for propagation to subsequent generations. We found that haplotypes consistently increased in frequency when they were initially rare and decreased in frequency when initially common. Our results have important implications for the use of mtDNA haplotype frequency data to infer population level processes and they revive the general hypothesis that negative frequency-dependent selection, presumably caused by habitat heterogeneity, may commonly promote polymorphism in ecologically relevant life history genes.

The influence of mitonuclear genetic variation on personality in seed beetles.

There is a growing awareness of the influence of mitochondrial genetic variation on life-history phenotypes, particularly via epistatic interactions with nuclear genes. Owing to their direct effect on traits such as metabolic and growth rates, mitonuclear interactions may also affect variation in behavioural types or personalities (i.e. behavioural variation that is consistent within individuals, but differs among individuals). However, this possibility is largely unexplored. We used mitonuclear introgression lines, where three mitochondrial genomes were introgressed into three nuclear genetic backgrounds, to disentangle genetic effects on behavioural variation in a seed beetle. We found within-individual consistency in a suite of activity-related behaviours, providing evidence for variation in personality. Composite measures of overall activity of individuals in behavioural assays were influenced by both nuclear genetic variation and by the interaction between nuclear and mitochondrial genomes. More importantly, the degree of expression of behavioural and life-history phenotypes was correlated and mitonuclear genetic variation affected expression of these concerted phenotypes. These results show that mitonuclear genetic variation affects both behavioural and life-history traits, and they provide novel insights into the maintenance of genetic variation in behaviour and personality.

Ejaculate Allocation and Sperm Characteristics Differ among Alternative Male Types in a Species of Fish with Cooperation and Competition among Unrelated Males.

Sexual selection arising from sperm competition has driven the evolution of immense variation in ejaculate allocation and sperm characteristics not only among species, but also among males within a species. One question that has received little attention is how cooperation among males affects these patterns. Here we ask how male alternative reproductive types differ in testes size, ejaculate production, and sperm morphology in the ocellated wrasse, a marine fish in which unrelated males cooperate and compete during reproduction. Nesting males build nests, court females and provide care. Sneaker males only "sneak" spawn, while satellite males sneak, but also help by chasing away sneakers. We found that satellite males have larger absolute testes than either sneakers or nesting males, despite their cooperative role. Nesting males invested relatively less in testes than either sneakers or satellites. Though sneakers produced smaller ejaculates than either satellite or nesting males, we found no difference among male types in either sperm cell concentration or sperm number, implying sneakers may produce less seminal fluid. Sperm tail length did not differ significantly among male types, but sneaker sperm cells had significantly larger heads than either satellite or nesting male sperm, consistent with past research showing sneakers produce slower sperm. Our results highlight that social interactions among males can influence sperm and ejaculate production.

Costs of changing sex do not explain why sequential hermaphroditism is rare.

Sex change is a relatively rare phenomenon among animals. While classic theory has been successful in assessing the adaptive significance of sex change and predicting within-species patterns, it does not explain why more animals are not sex changers. A possible explanation for the rarity of sex change is that costs such as decreased reproduction due to gonadal reconstruction favor separate sexes, or dioecy. These costs, however, have not been studied empirically or theoretically. Here, we investigate whether costs of changing sex can favor dioecy. Our analyses suggest that dioecy is favored only when costs of changing sex are large. Moreover, the fitness effect of costs and the strength of male size advantage are not static but change with the population composition, resulting in a dynamic evolutionary game between sex change and dioecy. We conclude that costs of changing sex alone are unlikely to explain the observed rarity of sex changers. Instead, assessing mating systems comparatively and quantitatively and identifying correlates selecting for and against sex change are necessary to understand why some species change sex while others do not.

Influence of sexual selection and feeding functional morphology on diversification rate of parrotfishes (Scaridae).

Scaridae (parrotfishes) is a prominent clade of 96 species that shape coral reef communities worldwide through their actions as grazing herbivores. Phylogenetically nested within Labridae, the profound ecological impact and high species richness of parrotfishes suggest that their diversification and ecological success may be linked. Here, we ask whether parrotfish evolution is characterized by a significant burst of lineage diversification and whether parrotfish diversity is shaped more strongly by sexual selection or modifications of the feeding mechanism. We first examined scarid diversification within the greater context of labrid diversity. We used a supermatrix approach for 252 species to propose the most extensive phylogenetic hypothesis of Labridae to date, and time-calibrated the phylogeny with fossil and biogeographical data. Using divergence date estimates, we find that several parrotfish clades exhibit the highest diversification rates among all labrid lineages. Furthermore, we pinpoint a rate shift at the shared ancestor of Scarus and Chlorurus, a scarid subclade characterized by territorial behaviour and strong sexual dichromatism, suggesting that sexual selection was a major factor in parrotfish diversification. Modifications of the pharyngeal and oral jaws that happened earlier in parrotfish evolution may have contributed to this diversity by establishing parrotfishes as uniquely capable reef herbivores.

The evolution of optimal female mating rate changes the coevolutionary dynamics of female resistance and male persistence.

Mating decisions usually involve conflict of interests between sexes. Accordingly, males benefit from increased number of matings, whereas costs of mating favour a lower mating rate for females. The resulting sexual conflict underlies the coevolution of male traits that affect male mating success ('persistence') and female traits that affect female mating patterns ('resistance'). Theoretical studies on the coevolutionary dynamics of male persistence and female resistance assumed that costs of mating and, consequently, the optimal female mating rate are evolutionarily constant. Costs of mating, however, are often caused by male 'persistence' traits that determine mating success. Here, we present a model where the magnitude of costs of mating depend on, and evolve with, male persistence. We find that allowing costs of mating to depend on male persistence results in qualitatively different coevolutionary dynamics. Specifically, we find that male traits such as penis spikes that harm females are not predicted to exhibit runaway selection with female resistance, in contrast to previous theory that predicts indefinite escalation. We argue that it is essential to determine when and to what extent costs of mating are caused by male persistence in order to understand and accurately predict coevolutionary dynamics of traits involved in mating decisions.

The evolution of social interactions changes predictions about interacting phenotypes.

In many traits involved in social interactions, such as courtship and aggression, the phenotype is an outcome of interactions between individuals. Such traits whose expression in an individual is partly determined by the phenotype of its social partner are called "interacting phenotypes." Quantitative genetic models suggested that interacting phenotypes can evolve much faster than nonsocial traits. Current models, however, consider the interaction between phenotypes of social partners as a fixed phenotypic response rule, represented by an interaction coefficient (ψ). Here, we extend existing theoretical models and incorporate the interaction coefficient as a trait that can evolve. We find that the evolution of the interaction coefficient can change qualitatively the predictions about the rate and direction of evolution of interacting phenotypes. We argue that it is crucial to determine whether and how the phenotypic response of an individual to its social partner can evolve to make accurate predictions about the evolution of traits involved in social interactions.

A comparative analysis of sex change in Labridae supports the size advantage hypothesis.

The size advantage hypothesis (SAH) predicts that the rate of increase in male and female fitness with size (the size advantage) drives the evolution of sequential hermaphroditism or sex change. Despite qualitative agreement between empirical patterns and SAH, only one comparative study tested SAH quantitatively. Here, we perform the first comparative analysis of sex change in Labridae, a group of hermaphroditic and dioecious (non-sex changer) fish with several model sex-changing species. We also estimate, for the first time, rates of evolutionary transitions between sex change and dioecy. Our analyses support SAH and indicate that the evolution of hermaphroditism is correlated to the size advantage. Furthermore, we find that transitions from sex change to dioecy are less likely under stronger size advantage. We cannot determine, however, how the size advantage affects transitions from dioecy to sex change. Finally, contrary to what is generally expected, we find that transitions from dioecy to sex change are more likely than transitions from sex change to dioecy. The similarity of sexual differentiation in hermaphroditic and dioecious labrids might underlie this pattern. We suggest that elucidating the developmental basis of sex change is critical to predict and explain patterns of the evolutionary history of sequential hermaphroditism.

Functional innovations and morphological diversification in parrotfish.

The association between diversification and evolutionary innovations has been well documented and tested in studies of taxonomic richness but the impact that such innovations have on the diversity of form and function is less well understood. Using phylogenetically rigorous techniques, we investigated the association between morphological diversity and two design breakthroughs within the jaws of parrotfish. Similar intramandibular joints and other modifications of the pharyngeal jaws have evolved repeatedly in teleost fish and are frequently hypothesized to promote diversity. We quantified morphological diversity within six functionally important oral jaw traits using the Brownian motion rate of evolution to correct for phylogenetic and time-related biases and compared these rates across clades that did and did not possess the intramandibular joint and the parrotfish pharyngeal jaw. No change in morphological diversity was associated with the pharyngeal jaw modification alone but rates of oral jaw diversification were up to 8× faster in parrotfish species that possessed both innovations. Interestingly, this morphological diversity may not have led to differential resource uses as available data suggest that members of this clade show remarkable homogeneity of diet.