Sex-dependent selection differentially shapes genetic variation on and off the guppy Y chromosome

Because selection is often sex-dependent, alleles can have positive effects on fitness in one sex and negative effects in the other, resulting in intralocus sexual conflict. Evolutionary theory predicts that intralocus sexual conflict can drive the evolution of sex limitation, sex-linkage, and sex chromosome differentiation. However, evidence that sex-dependent selection results in sex-linkage is limited. Here, we formally partition the contribution of Y-linked and non-Y-linked quantitative genetic variation in coloration, tail, and body size of male guppies (Poecilia reticulata)—traits previously implicated as sexually antagonistic. We show that these traits are strongly genetically correlated, both on and off the Y chromosome, but that these correlations differ in sign and magnitude between both parts of the genome. As predicted, variation in attractiveness was found to be associated with the Y-linked, rather than with the non-Y-linked component of genetic variation in male ornamentation. These findings show how the evolution of Y-linkage may be able to resolve sexual conflict. More generally, they provide unique insight into how sex-specific selection has the potential to differentially shape the genetic architecture of fitness traits across different parts of the genome.

Experimental reduction in dietary omega-3 polyunsaturated fatty acids depresses sperm competitiveness

 The health benefits of diets containing rich sources of long-chain omega-3 polyunsaturated fatty acids (n-3 LC-PUFA) are well documented and include reductions in the risk of several diseases typical of Western societies. The dietary intake of n-3 LC-PUFA has also been linked to fertility, and there is abundant evidence that a range of ejaculate traits linked to fertility in humans, livestock and other animals depend on an adequate intake of n-3 LC-PUFA from dietary sources. However, relatively few studies have explored how n-3 LC-PUFA influence reproductive fitness, particularly in the context of sexual selection. Here, we show that experimental reduction in the level of n-3 LC-PUFA in the diet of guppies (Poecilia reticulata) depresses a male’s share of paternity when sperm compete for fertilization, confirming that the currently observed trend for reduced n-3 LC-PUFA in western diets has important implications for individual reproductive fitness.

A new light on sex: signalling in the guppy

The environment influences the evolution of animal colour signals in highly complex ways. This PhD identified the effects of varying light environments on the evolution of colour signals, identified behaviours that are able to mitigate these effects and demonstrated co-option as a potential origin of colour sexual signals.

Variable environmental effects on a multicomponent sexually selected trait

Multicomponent signals are made up of interacting elements that generate a functional signaling unit. The interactions between signal components and their effects on individual fitness are not well understood, and the effect of environment is even less so. It is usually assumed that color patterns appear the same in all light environments and that the effects of each color are additive. Using guppies, Poecilia reticulata, we investigated the effect of water color on the interactions between components of sexually selected male coloration. Through behavioral mate choice trials in four different water colors, we estimated the attractiveness of male color patterns, using multivariate fitness estimates and overall signal contrast. Our results show that females exhibit preferences that favor groups of colors rather than individual colors independently and that each environment favors different color combinations. We found that these effects are consistent with female guppies selecting entire color patterns on the basis of overall visual contrast. This suggests that both individuals and populations inhabiting different light environments will be subject to divergent, multivariate selection. Although the appearance of color patterns changes with light environment, achromatic components change little, suggesting that these could function in species recognition or other aspects of communication that must work across environments. Consequently, we predict different phylogenetic patterns between chromatic and achromatic signals within the same clades.

Social networks in changing environments

Social network analysis (SNA) has become a widespread tool for the study of animal social organisation. However despite this broad applicability, SNA is currently limited by both an overly strong focus on pattern analysis as well as a lack of dynamic interaction models. Here, we use a dynamic modelling approach that can capture the responses of social networks to changing environments. Using the guppy, Poecilia reticulata, we identified the general properties of the social dynamics underlying fish social networks and found that they are highly robust to differences in population density and habitat changes. Movement simulations showed that this robustness could buffer changes in transmission processes over a surprisingly large density range. These simulation results suggest that the ability of social systems to self-stabilise could have important implications for the spread of infectious diseases and information. In contrast to habitat manipulations, social manipulations (e.g. change of sex ratios) produced strong, but short-lived, changes in network dynamics. Lastly, we discuss how the evolution of the observed social dynamics might be linked to predator attack strategies. We argue that guppy social networks are an emergent property of social dynamics resulting from predator–prey co-evolution. Our study highlights the need to develop dynamic models of social networks in connection with an evolutionary framework.

Male courtship decisions are influenced by light environment and female receptivity.

The appearance of animal colour signals depends jointly upon the ambient light spectrum and the signal's reflectance spectra. Light environment heterogeneity might, therefore, allow individuals to enhance their signal by signalling in an environment that increases signal efficacy. We tested this hypothesis by providing male guppies (Poecilia reticulata), a choice of three light environments in which to display their colour signal to females: green, lilac, and clear. We paired males with both receptive and non-receptive females to test whether female response might affect male behavioural decisions. Males preferred the clear environment in all trials and this environment also resulted in males having the highest average visual contrast. Sexual behaviour was influenced by complex interactions between female receptivity, light environment, and male colour pattern contrast. Males spent significantly more time in the environment in which their colour signal had the highest contrast, but only when paired with receptive females. Significant interactions between light environment and individual male colour components were also seen only in receptive trials. Our results suggest that males use light environment to enhance their colour pattern, but only in the presence of receptive females.

Towards powerful experimental and statistical approaches to study intraindividual variability in labile traits

There is a long-standing interest in behavioural ecology, exploring the causes and correlates of consistent individual differences in mean behavioural traits ('personality') and the response to the environment ('plasticity'). Recently, it has been observed that individuals also consistently differ in their residual intraindividual variability (rIIV). This variation will probably have broad biological and methodological implications to the study of trait variation in labile traits, such as behaviour and physiology, though we currently need studies to quantify variation in rIIV, using more standardized and powerful methodology. Focusing on activity rates in guppies (Poecilia reticulata), we provide a model example, from sampling design to data analysis, in how to quantify rIIV in labile traits. Building on the doubly hierarchical generalized linear model recently used to quantify individual differences in rIIV, we extend the model to evaluate the covariance between individual mean values and their rIIV. After accounting for time-related change in behaviour, our guppies substantially differed in rIIV, and it was the active individuals that tended to be more consistent (lower rIIV). We provide annotated data analysis code to implement these complex models, and discuss how to further generalize the model to evaluate covariances with other aspects of phenotypic variation.