Sex-specific behavioral syndromes allow the independent evolution of behavioral dimorphism

When selection differs by sex, the capacity for sexes to reach optimal phenotypes can be constrained by the shared genome of males and females. Because phenotypic traits are often correlated, this difference extends across multiple traits and underlying genetic correlations can further constrain evolutionary responses. Behaviors are frequently correlated as behavioral syndromes, and these correlations often have a genetic basis. However, whether cross-sex and across behavior correlations lead constrained evolution remains unknown. Here, we show that a boldness-activity syndrome is strongly sex-specific at the genetic level in the western field cricket (Gryllus integer) and that emergence from a shelter is genetically independent between males and females. However, male activity is strongly related to female shelter emergence, creating the potential for biased responses to selection. Our results show that the sex-specific genetic architecture of behavioral syndromes can shape the evolution of behavioral phenotypes.

Behavioural syndromes shape evolutionary trajectories via conserved genetic architecture

Behaviours are often correlated within broader syndromes, creating the potential for evolution in one behaviour to drive evolutionary changes in other behaviours. Despite demonstrations that behavioural syndromes are common, this potential for evolutionary effects has not been demonstrated. Here we show that populations of field crickets ( Gryllus integer ) exhibit a genetically conserved behavioural syndrome structure, despite differences in average behaviours. We found that the distribution of genetic variation and genetic covariance among behavioural traits was consistent with genes and cellular mechanisms underpinning behavioural syndromes rather than correlated selection. Moreover, divergence among populations' average behaviours was constrained by the genetically conserved behavioural syndrome. Our results demonstrate that a conserved genetic architecture linking behaviours has shaped the evolutionary trajectories of populations in disparate environments—illustrating an important way for behavioural syndromes to result in shared evolutionary fates.

Behavioral syndromes shape evolutionary trajectories via conserved genetic architecture

Behaviors are often correlated within broader syndromes, creating the potential for evolution in one behavior to drive evolutionary changes in other behaviors. Despite demonstrations that behavioral syndromes are common across taxa, whether this potential for evolutionary effects is realized has not yet been demonstrated. Here we show that populations of field crickets (Gryllus integer) exhibit a genetically conserved behavioral syndrome structure despite differences in average behaviors. We found that the distribution of genetic variation and genetic covariance among behavioral traits was consistent with genes and cellular mechanisms underpinning behavioral syndromes rather than correlated selection. Moreover, divergence among populations’ average behaviors was constrained by the genetically conserved behavioral syndrome. Our results demonstrate that a conserved genetic architecture linking behaviors has shaped the evolutionary trajectories of populations in disparate environments—illustrating an important way by which behavioral syndromes result in shared evolutionary fates.

Metabolic rate associates with, but does not generate covariation between, behaviours in western stutter-trilling crickets, Gryllus integer

The causes and consequences of among-individual variation and covariation in behaviours are of substantial interest to behavioural ecology, but the proximate mechanisms underpinning this (co)variation are still unclear. Previous research suggests metabolic rate as a potential proximate mechanism to explain behavioural covariation. We measured the resting metabolic rate (RMR), boldness and exploration in western stutter-trilling crickets, Gryllus integer , selected differentially for short and fast development over two generations. After applying mixed-effects models to reveal the sign of the covariation, we applied structural equation models to an individual-level covariance matrix to examine whether the RMR generates covariation between the measured behaviours. All traits showed among-individual variation and covariation: RMR and boldness were positively correlated, RMR and exploration were negatively correlated, and boldness and exploration were negatively correlated. However, the RMR was not a causal factor generating covariation between boldness and exploration. Instead, the covariation between all three traits was explained by another, unmeasured mechanism. The selection lines differed from each other in all measured traits and significantly affected the covariance matrix structure between the traits, suggesting that there is a genetic component in the trait integration. Our results emphasize that interpretations made solely from the correlation matrix might be misleading.

Dominance is not always an honest signal of male quality, but females may be able to detect the dishonesty

Females prefer dominant males as mating partners in numerous species. Male dominance rank is considered as an honest signal of male quality, because only healthy males in good condition are thought to be able to win fights with other males. Here, we tested whether activation of the immune system influences the success of males in male–male competition and mating in the field cricket, Gryllus integer . We activated the immune system of males with a nylon monofilament (to mimic a parasitoid larva), and arranged fights between male pairs to assess male dominance and associated mating success. Activation of the immune system with nylon monofilament substantially enhanced the fighting success of males during male–male competition but had no effect on mating success. However, sham-manipulation (a wound only) did not have any effect on fighting success although females mated more often with dominant males. Our study suggests that when male crickets meet an apparent survival threat they may behave more dominantly, probably owing to terminal investment. Male success during male–male competition is not always an honest signal of males’ quality, but females may be able to detect this dishonesty.