Environmental influences on for-mediated oviposition decisions in Drosophila melanogaster.

Deciding whether or not to lay an egg on a given substrate is an important task undertaken by females of many arthropods. It involves perceiving the environment (e.g. quality of the substrate, temperature, and humidity), formulating a decision, and then conducting the appropriate behaviours to oviposit. This oviposition site selection (OSS) provides a useful system for studying simple decision-making. OSS in fruit flies, Drosophila melanogaster, is influenced by both genetic and environmental variation. Naturally occurring allelic variation in the foraging gene (for) is known to affect OSS. Given a choice of high- and low-nutrient oviposition substrates, groups of rovers (forR) are known to lay significantly more of their eggs on low-nutrient sites than sitters (fors) and sitter mutants (fors2). Here we ask three questions: (1) Is the role of for in OSS affected by the availability of alternate oviposition sites? (2) Is the role of for in OSS sensitive to the density of ovipositing females? and (3) Does the gustatory sensation of yeast play a role in for-mediated variation in OSS? We find a role of choice and female density in rover/sitter differences in OSS, as well as a role of for in response to glycerol, an indicator of yeast. The role of for in OSS decision-making is complex and multi-faceted and should prove fertile ground for further research into the factors affecting decision-making behaviours.

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.

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.

Evolutionary adaptation to climate change.

When the notion of climate change emerged over 200 years ago, few speculated as to the impact of rising atmospheric temperatures on biological life. Tens of decades later, research clearly demonstrates that the impact of climate change on life on Earth is enormous, ongoing, and with foreseen effects lasting well into the next century. Responses to climate change have been widely documented. However, the breadth of phenotypic traits involved with evolutionary adaptation to climate change remains unclear. In addition, it is difficult to identify the genetic and/or epigenetic bases of phenotypes adaptive to climate change, in part because it often is not clear whether this change is plastic, genetic, or some combination of the two. Adaptive responses to climate-driven selection also interact with other processes driving genetic changes in general, including demography as well as selection driven by other factors. In this Special Issue, we explore the factors that will impact the overall outcome of climate change adaptation. Our contributions explain that traits involved in climate change adaptation include not only classic phenomena, such as range shifts and environmentally dependent sex determination, but also often overlooked phenomena such as social and sexual conflicts and the expression of stress hormones. We learn how climate-driven selection can be mediated via both natural and sexual selection, effectively influencing key fitness-related traits such as offspring growth and fertility as well as evolutionary potential. Finally, we explore the limits and opportunities for predicting adaptive responses to climate change. This contribution forms the basis of 10 actions that we believe will improve predictions of when and how organisms may adapt genetically to climate change. We anticipate that this Special Issue will inform novel investigations into how the effects of climate change unfold from phenotypes to genotypes, particularly as methodologies increasingly allow researchers to study selection in field experiments.

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 (for(s) and for(R)) 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.

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.

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.

'Foraging' for a place to lay eggs: A genetic link between foraging behaviour and oviposition preferences.

Gravid female arthropods in search of egg-laying substrates embark on foraging-like forays: they survey the environment assessing multiple patches, tasting each with their tarsi and proboscis, and then, if interested, they deposit an egg (or eggs). In fruit flies, Drosophila melanogaster, allelic variation in the foraging gene (for) underlies the rover/sitter foraging behaviour polymorphism. Rover flies (forR) are more active foragers (both within and between food patches) compared to sitters (fors). In nematodes, Caenorhabditis elegans, a mutation in egl-4, the ortholog of for, leads to aberrations in egg laying. Given this and the notion that females may 'forage' for a place to oviposit, we hypothesized that for may underlie egg-laying decisions in the fruit fly. Indeed, when given a choice between patches of low- and high-nutrient availability, rovers lay significantly more eggs on the low-nutrient patches than sitters and also a sitter mutant (fors2). We confirm the role of for by inducing rover-like oviposition preferences in a sitter fly using the transgenic overexpression of for-mRNA in the nervous system.

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.

Candidate genes for behavioural ecology.

In spite of millions of years of evolutionary divergence, the conservation of gene function is common across distant lineages. As such, genes that are known to influence behaviour in one organism are likely to influence similar behaviours in other organisms. Recent studies of the evolution of behaviour and morphological adaptation support this notion. Thus, the candidate gene approach offers great potential to expand our understanding of behavioural ecology. Changes in the expression of candidate genes can reveal their contribution to behavioural variation and/or phenotypic plasticity. Knowledge of gene function also enables experimental manipulation of behaviour in the lab and in the field. The candidate gene approach provides an accessible and useful tool for generating insights about animals that are not typically associated with genetic experimentation.

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

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.