Mark J. Fitzpatrick

Maintaining a behaviour polymorphism by frequency-dependent selection on a single gene.

Accounting for the abundance of genetic variation in the face of natural selection remains a central problem of evolutionary biology. Genetic polymorphisms are constantly arising through mutation, and although most are promptly eliminated, polymorphisms in functionally important traits are common. One mechanism that can maintain polymorphisms is negative frequency-dependent selection on alternative alleles, whereby the fitness of each decreases as its frequency increases. Examples of frequency-dependent selection are rare, especially when attempting to describe the genetic basis of the phenotype under selection. Here we show frequency-dependent selection in a well-known natural genetic polymorphism affecting fruitfly foraging behaviour. When raised in low nutrient conditions, both of the naturally occurring alleles of the foraging gene (fors and forR) have their highest fitness when rare—the hallmark of negative frequency-dependent selection. This effect disappears at higher resources levels, demonstrating the role of larval competition. We are able to confirm the involvement of the foraging gene by showing that a sitter-like mutant allele on a rover background has similar frequency-dependent fitness as the natural sitter allele. Our study represents a clear demonstration of frequency-dependent selection, and we are able to attribute this effect to a single, naturally polymorphic gene known to affect behaviour.

Pleiotropy and the Genomic Location of Sexually Selected Genes

Sexual selection drives the evolution of traits involved in the competition for mates. Although considerable research has focused on the evolution of sexually selected traits, their underlying genetic architecture is poorly resolved. Here I address the pleiotropic effects and genomic locations of sexually selected genes. These two important characteristics can impose considerable constraints on evolvability and may influence our understanding of the process of sexual selection. Theoretical models are inconsistent regarding the genomic location of sexually selected genes. Models that do not incorporate pleiotropic effects often predict sex linkage. Conversely, sex linkage is not explicitly predicted by the condition‐dependent model (which considers pleiotropic effects). Evidence largely based on reciprocal crosses supports the notion of sex linkage. However, although they infer genetic contribution, reciprocal crosses cannot identify the genes or their pleiotropic effects. By surveying the genome of Drosophila melanogaster, I provide evidence for the genomic location and pleiotropic effects of 63 putatively sexually selected genes. Interestingly, most are pleiotropic (73%), and they are not preferentially sex linked. Their pleiotropic effects include fertility, development, life span, and viability, which may contribute to condition and/or fitness. My findings may also provide evidence for the capture of genetic variation in condition via the pleiotropic effects of sexually selected genes.

In Search of Food: Exploring the Evolutionary Link Between cGMP-Dependent Protein Kinase (PKG) and Behaviour

Abstract Despite an immense amount of variation in organisms throughout the animal kingdom many of their genes show substantial conservation in DNA sequence and protein function. Here we explore the potential for a conserved evolutionary relationship between genes and their behavioural phenotypes. We investigate the evolutionary history of cGMP-dependent protein kinase (PKG) and its possible conserved function in food-related behaviours. First identified for its role in the foraging behaviour of fruit flies, the PKG encoded by the foraging gene has since been associated with the maturation of behaviour (from nurse to forager) in honey bees and the roaming and dwelling food-related locomotion in nematodes. These parallels encouraged us to construct protein phylogenies using 32 PKG sequences that include 19 species. Our analyses suggest five possible evolutionary histories that can explain the apparent conserved link between PKG and behaviour in fruit flies, honey bees and nematodes. Three of these raise the hypothesis that PKG influences the food-related behaviours of a wide variety of animals including vertebrates. Moreover, it appears that the PKG gene was duplicated some time between the evolution of nematodes and a common ancestor of vertebrates and insects whereby current evidence suggests only the for-like PKG might be associated with food-related behaviour.

Alleles underlying larval foraging behaviour influence adult dispersal in nature.

The dispersal and migration of organisms have resulted in the colonisation of nearly every possible habitat and ultimately the extraordinary diversity of life. Animal dispersal tendencies are commonly heterogeneous (e.g. long vs. short) and non-random suggesting that phenotypic and genotypic variability between individuals can contribute to population-level heterogeneity in dispersal. Using laboratory and field experiments, we demonstrate that natural allelic variation in a gene underlying a foraging polymorphism in larval fruit flies (for), also influences their dispersal tendencies as adults. Rover flies (for(R) ; higher foraging activity) have consistently greater dispersal tendencies and are more likely to disperse longer distances than sitter flies (for(s) ; lower foraging activity). Increasing for expression in the brain and nervous system increases dispersal in sitter flies. Our study supports the notion that variation in dispersal can be driven by intrinsic variation in food-dependent search behaviours and confirms that single gene pleiotropic effects can contribute to population-level heterogeneity in dispersal.

A lover, not a fighter: mating causes male crickets to lose fights

Both resource-holding potential (RHP) and experience in aggressive contests are known to affect future aggressive behaviour. However, few studies have examined the effects of mating experience on agonistic behaviour, despite the fact that dominant males usually acquire more matings. We investigated the effect of mating experience on male aggressive behaviour including the relationship between RHP and fighting success in the fall field cricket, Gryllus pennsylvanicus. We formed pairs of size- and age-matched males that varied in RHP (relative weapon size) and conducted two experiments. In the first, we varied male mating experience by allowing one male in a pair to either be (a) ‘mated’: court, be mounted and copulate with a virgin female or (b) ‘experienced’: court, be mounted, but prevented from copulating. The second experiment varied postcopulatory experience where the male was allowed (‘contact’) or prevented from (‘no-contact’) continued contact with his recent mate. Following treatment, experimental males engaged in an aggressive contest with the naïve size- and age-matched male. In our first experiment, we found that mated and experienced males were equally likely to escalate contests to combat with a naïve opponent, but mated males were less likely than experienced males to win. There was no effect of mating on the relationship between RHP and fighting success. In our second experiment, we found no effect of maintaining contact with the female on the tendency to escalate or the probability of winning. As in the first experiment, males with relatively larger heads again won more fights and this relationship was unaffected by male experience. These results suggest that mating is itself detrimental to male success in aggressive contests, but that this effect is not sufficient to eliminate the effect of RHP on fighting success.

Experimental evidence for the effect of habitat loss on the dynamics of migratory networks

Migratory animals present a unique challenge for understanding the consequences of habitat loss on population dynamics because individuals are typically distributed over a series of interconnected breeding and non-breeding sites (termed migratory network). Using replicated breeding and non-breeding populations of Drosophila melanogaster and a mathematical model, we investigated three hypotheses to explain how habitat loss influenced the dynamics of populations in networks with different degrees of connectivity between breeding and non-breeding seasons. We found that habitat loss increased the degree of connectivity in the network and influenced population size at sites that were not directly connected to the site where habitat loss occurred. However, connected networks only buffered global population declines at high levels of habitat loss. Our results demonstrate why knowledge of the patterns of connectivity across a species range is critical for predicting the effects of environmental change and provide empirical evidence for why connected migratory networks are commonly found in nature.

The genomics of climate change

A study of yellow warblers identifies genomic regions involved in climate change adaptation Human-induced climate change is causing rapidly changing global temperatures and extreme fluctuations in precipitation. These changes force organisms to adapt and evolve or face extinction. Understanding and predicting the evolutionary responses to climate change is critical for preserving biodiversity, but predictions are challenging because they involve interactions between adaptive plasticity (such as altered breeding times) and evolved responses (such as increased metabolism). On page 83 of this issue, Bay et al. (1) combine high-resolution genomic sequencing with population trends and global climate predictions to estimate the adaptive potential (that is, the genetic variation necessary for adaptation) of yellow warblers (see the photo) to climate change and predict future population declines. In doing so, they produce a powerful tool for estimating genomic vulnerability to climate change and locate candidate genes that are key for climate change adaptation.

Behavioural Genetics: Worms Seek That Old Beetle Smell

Some nematodes eavesdrop on pheromonal signals to sniff out their elderly beetle hosts. This turns out to be yet another behaviour regulated by cGMP/PKG signalling.

Habitat connectivity is determined by the scale of habitat loss and dispersal strategy

Abstract Understanding factors that ameliorate the impact of habitat loss is a major focus of conservation research. One key factor influencing species persistence and evolution is the ability to disperse across increasingly patchy landscapes. Here we ask whether interpatch distance (a proxy for habitat loss) and dispersal strategy can interact to form thresholds where connectivity breaks down. We assayed dispersal across a range of interpatch distances in fruit flies carrying allelic variants of a gene known to underlie differences in dispersal strategy. Dispersal‐limited flies experienced a distinct negative threshold in connectivity at greater interpatch distances, and this was not observed in more dispersive flies. Consequently, this differential response of dispersal‐limited and more dispersive flies to decreasing connectivity suggests that habitat loss could have important implications on the evolution and maintenance of genetic variation underlying dispersal strategy.