Parent-offspring conflict and co-adaptation: behavioural ecology meets quantitative genetics

The evolution of the complex and dynamic behavioural interactions between caring parents and their dependent offspring is a major area of research in behavioural ecology and quantitative genetics. While behavioural ecologists examine the evolution of interactions between parents and offspring in the light of parent-offspring conflict and its resolution, quantitative geneticists explore the evolution of such interactions in the light of parent-offspring co-adaptation due to combined effects of parental and offspring behaviours on fitness. To date, there is little interaction or integration between these two fields. Here, we first review the merits and limitations of each of these two approaches and show that they provide important complementary insights into the evolution of strategies for offspring begging and parental resource provisioning. We then outline how central ideas from behavioural ecology and quantitative genetics can be combined within a framework based on the concept of behavioural reaction norms, which provides a common basis for behavioural ecologists and quantitative geneticists to study the evolution of parent-offspring interactions. Finally, we discuss how the behavioural reaction norm approach can be used to advance our understanding of parent-offspring conflict by combining information about the genetic basis of traits from quantitative genetics with key insights regarding the adaptive function and dynamic nature of parental and offspring behaviours from behavioural ecology.     

Brain evolution by brain pathway duplication

Understanding the mechanisms of evolution of brain pathways for complex behaviours is still in its infancy. Making further advances requires a deeper understanding of brain homologies, novelties and analogies. It also requires an understanding of how adaptive genetic modifications lead to restructuring of the brain. Recent advances in genomic and molecular biology techniques applied to brain research have provided exciting insights into how complex behaviours are shaped by selection of novel brain pathways and functions of the nervous system. Here, we review and further develop some insights to a new hypothesis on one mechanism that may contribute to nervous system evolution, in particular by brain pathway duplication. Like gene duplication, we propose that whole brain pathways can duplicate and the duplicated pathway diverge to take on new functions. We suggest that one mechanism of brain pathway duplication could be through gene duplication, although other mechanisms are possible. We focus on brain pathways for vocal learning and spoken language in song-learning birds and humans as example systems. This view presents a new framework for future research in our understanding of brain evolution and novel behavioural traits.     

An overview of the utility of population simulation software in molecular ecology

Stochastic simulation software that simultaneously model genetic, population and environmental processes can inform many topics in molecular ecology. These include forecasting species and community response to environmental change, inferring dispersal ecology, revealing cryptic mating, quantifying past population dynamics, assessing in situ management options and monitoring neutral and adaptive biodiversity change. Advances in population demographic–genetic simulation software, especially with respect to individual life history, landscapes and genetic processes, are transforming and expanding the ways that molecular data can be used. The aim of this review is to explain the roles that such software can play in molecular ecology studies (whether as a principal component or a supporting function) so that researchers can decide whether, when and precisely how simulations can be incorporated into their work. First, I use seven case studies to demonstrate how simulations are employed, their specific advantage/necessity and what alternative or complementary (nonsimulation) approaches are available. I also explain how simulations can be integrated with existing spatial, environmental, historical and genetic data sets. I next describe simulation features that may be of interest to molecular ecologists, such as spatial and behavioural considerations and species' interactions, to provide guidance on how particular simulation capabilities can serve particular needs. Lastly, I discuss the prospect of simulation software in emerging challenges (climate change, biodiversity monitoring, population exploitation) and opportunities (genomics, ancient DNA), in order to emphasize that the scope of simulation‐based work is expanding. I also suggest practical considerations, priorities and elements of best practice. This should accelerate the uptake of simulation approaches and firmly embed them as a versatile tool in the molecular ecologist's toolbox.     

Implications of flexible foraging for interspecific interactions: lessons from simple models

1.  Some types of flexible foraging behaviours were incorporated into ecological thought in the 1960s, but the population dynamical consequences of such behaviours are still poorly understood.
2.  Flexible foraging-related traits can be classified as shifts in general and specific foraging effort, and shifts in general and specific defense.
3.  Many flexible foraging behaviours suggested by theory have received very little empirical attention, and empirical techniques used to compare the magnitudes of behavioural and non-behavioural responses to predation are likely to have overestimated the behavioural components.
4.  Adaptively flexible foraging in theory causes significant changes in the forms of consumer functional responses and generates a variety of indirect interactions. These can alter fundamental ecological processes, such as co-existence of competitors, and top-down or bottom-up effects in food webs.
5.  Many aspects of flexible foraging are still largely unknown, including the issues of how to represent the dynamics of such phenotypically plastic traits, how flexible traits in multiple species interact, what types of adaptive movements occur in metacommunities, and how adaptive behaviours influence evolutionary change.
6.  Population dynamics in large food webs may be less dependent on behavioural flexibility than in small webs because species replacement may preempt some potential types of behavioural change within species.     

Behaviour genetics ofDrosophila: Non-sexual behaviour

The analysis of genetic behaviour within and between species provides important clues about the forces shaping the evolution of behavioural genes. Genes can affect natural behavioural variation in different ways. Allelic variation causes alternative behavioural phenotypes, whereas changes in gene expression can influence the initiation of behaviour at different ages. Identifying the genes involved in polygenic traits has been difficult. Chromosomal analysis has been widely used as a first step in elucidating the genetic architecture of several behaviours ofDrosophila. Behavioural genetic and molecular studies helped to reveal the genetic basis of circadian time keeping and rhythmic behaviours. InDrosophila, a number of key processes such as emergence from the pupal case, locomotor activity, feeding, olfaction and aspects of mating behaviour are under circadian regulation. Evolutionary biology considers migration behaviour as central in genetic structure of populations and speciation. Genetic loci that influence behaviour are often difficult to identify and localise in part due to the quantitative nature of behavioural phenotypes. Diapause is a hormonally mediated delayed response to future adverse conditions and can occur at any stage of development in an insect. Diapauseassociated gene expression was studied inDrosophila using subtractive hybridisation. Several approaches have been made to unravel the genetic complexity of the behaviour, which have provided information that may be useful in different ways. There is evidence that species do differ in genetic architecture of photoresponse and this may be related to their natural environment. The classical experiments by Jerry Hirsh and Th. Dobzhansky to know the nature of genetic basis for extreme selected geotactic behaviour in fruit flies constituted the first attempt at the genetic dissection of a complex, polygenic behaviour. Understanding the genetic differences between these selected lines would provide an important point of entry into the study of genetic mechanisms of sensing and responding to gravity, as well as clues to the origins of genetic flexibility and plasticity in an organism’s response.     

Effect of diet on the structure of animal personality

There is increasing interest in the proximate factors that underpin individual variation in suites of correlated behaviours. In this paper, we propose that dietary macronutrient composition, an underexplored environmental factor, might play a key role. Variation in macronutrient composition can lead to among-individual differentiation in single behaviours (‘personality’ ) as well as among-individual covariation between behaviours (‘behavioural syndromes’ ). Here, we argue that the nutritional balance during any life stage might affect the development of syndrome structure and the expression of genes with pleiotropic effects that influence development of multiple behaviours, hence genetic syndrome structure. We further suggest that males and females should typically differ in diet-dependent genetic syndrome structure despite a shared genetic basis. We detail how such diet-dependent multivariate gene-environment interactions can have major repercussions for the evolution of behavioural syndromes.     

Biphasic Retention of One-Trial Learning in a Clonal Fish (<Emphasis Type="Italic">Poecilia formosa</Emphasis>)

Most species used for behavioural studies are bisexual. Sexual dimorphism determines genotypic diversity and behavioural variation within a species. The relative contribution of a genome to a specific behaviour is for the most part indiscernible, but gene changes can alter behaviour in many different ways¹. Within a species, strain differences can contribute to behavioural differences and many less clearly systematic behaviours, such as the aptitude to learn or to recall, may be genetically determined². Genotypic diversity, on the other hand, obscures gene correlates of behaviour because each organism brings a unique repertoire of behaviours to the experimental situation. Against this, learning research has found basic phenomena of learning and memory to be valid across many vertebrate species. In an effort to reduce genotypic and behavioural variability in studying memory processing, we have used a unisexual clonal fish, Poecilia formosa, as suggested by Agranoff and Davis³.     

Genetics and developmental biology of cooperation

Despite essential progress towards understanding the evolution of cooperative behaviour, we still lack detailed knowledge about its underlying molecular mechanisms, genetic basis, evolutionary dynamics and ontogeny. An international workshop “Genetics and Development of Cooperation,” organized by the University of Bern (Switzerland), aimed at discussing the current progress in this research field and suggesting avenues for future research. This review uses the major themes of the meeting as a springboard to synthesize the concepts of genetic and nongenetic inheritance of cooperation, and to review a quantitative genetic framework that allows for the inclusion of indirect genetic effects. Furthermore, we argue that including nongenetic inheritance, such as transgenerational epigenetic effects, parental effects, ecological and cultural inheritance, provides a more nuanced view of the evolution of cooperation. We summarize those genes and molecular pathways in a range of species that seem promising candidates for mechanisms underlying cooperative behaviours. Concerning the neurobiological substrate of cooperation, we suggest three cognitive skills necessary for the ability to cooperate: (i) event memory, (ii) synchrony with others and (iii) responsiveness to others. Taking a closer look at the developmental trajectories that lead to the expression of cooperative behaviours, we discuss the dichotomy between early morphological specialization in social insects and more flexible behavioural specialization in cooperatively breeding vertebrates. Finally, we provide recommendations for which biological systems and species may be particularly suitable, which specific traits and parameters should be measured, what type of approaches should be followed, and which methods should be employed in studies of cooperation to better understand how cooperation evolves and manifests in nature.     

From kissing to belly stridulation: comparative analysis reveals surprising diversity,rapid evolution,and much homoplasy in the mating behaviour of 27 species of sepsid flies (Diptera: Sepsidae)

Our understanding of how fast mating behaviour evolves in insects is rather poor due to a lack of comparative studies among insect groups for which phylogenetic relationships are known. Here, we present a detailed study of the mating behaviour of 27 species of Sepsidae (Diptera) for which a well‐resolved and supported phylogeny is available. We demonstrate that mating behaviour is extremely diverse in sepsids with each species having its own mating profile. We define 32 behavioural characters and document them with video clips. Based on sister species comparisons, we provide several examples where mating behaviour evolves faster than all sexually dimorphic morphological traits. Mapping the behaviours onto the molecular tree reveals much homoplasy, comparable to that observed for third positions of mitochondrial protein‐encoding genes. A partitioned Bremer support (PBS) analysis reveals conflict between the molecular and behavioural data, but behavioural characters have higher PBS values per parsimony‐informative character than DNA sequence characters.     

Olfaction and olfactory-mediated behaviour in psychiatric disease models

Rats and mice are the most widely used species for modelling psychiatric disease. Assessment of these rodent models typically involves the analysis of aberrant behaviour with behavioural interactions often being manipulated to generate the model. Rodents rely heavily on their excellent sense of smell and almost all their social interactions have a strong olfactory component. Therefore, experimental paradigms that exploit these olfactory-mediated behaviours are among the most robust available and are highly prevalent in psychiatric disease research. These include tests of aggression and maternal instinct, foraging, olfactory memory and habituation and the establishment of social hierarchies. An appreciation of the way that rodents regulate these behaviours in an ethological context can assist experimenters to generate better data from their models and to avoid common pitfalls. We describe some of the more commonly used behavioural paradigms from a rodent olfactory perspective and discuss their application in existing models of psychiatric disease. We introduce the four olfactory subsystems that integrate to mediate the behavioural responses and the types of sensory cue that promote them and discuss their control and practical implementation to improve experimental outcomes. In addition, because smell is critical for normal behaviour in rodents and yet olfactory dysfunction is often associated with neuropsychiatric disease, we introduce some tests for olfactory function that can be applied to rodent models of psychiatric disorders as part of behavioural analysis.     

Personality and the emergence of the pace-of-life syndrome concept at the population level

The pace-of-life syndrome (POLS) hypothesis specifies that closely related species or populations experiencing different ecological conditions should differ in a suite of metabolic, hormonal and immunity traits that have coevolved with the life-history particularities related to these conditions. Surprisingly, two important dimensions of the POLS concept have been neglected: (i) despite increasing evidence for numerous connections between behavioural, physiological and life-history traits, behaviours have rarely been considered in the POLS yet; (ii) the POLS could easily be applied to the study of covariation among traits between individuals within a population. In this paper, we propose that consistent behavioural differences among individuals, or personality, covary with life history and physiological differences at the within-population, interpopulation and interspecific levels. We discuss how the POLS provides a heuristic framework in which personality studies can be integrated to address how variation in personality traits is maintained within populations.     

Future directions in behavioural syndromes research

A behavioural syndrome occurs when individuals behave in a consistent way through time or across contexts and is analogous to 'personality' or 'temperament'. Interest is accumulating in behavioural syndromes owing to their important ecological and evolutionary consequences. There are plenty of opportunities in this burgeoning young field to integrate proximate and functional approaches to studying behaviour, but there are few guidelines about where to start or how to design a study on behavioural syndromes. After summarizing what we do and do not know, this brief review aims to act as a general guide for studying behavioural syndromes. Although the array of possible behavioural combinations can seem overwhelming, there are at least four different strategies that can be used to choose which behaviours or contexts to study in a behavioural syndromes view. I describe the strengths and weaknesses of these non-exclusive strategies, and then discuss the methodological and statistical issues raised by such studies.     

Relationships between gene trees and species trees

It is well known that a phylogenetic tree (gene tree) constructed from DNA sequences for a genetic locus does not necessarily agree with the tree that represents the actual evolutionary pathway of the species involved (species tree). One of the important factors that cause this difference is genetic polymorphism in the ancestral species. Under the assumption of neutral mutations, this problem can be studied by evaluating the probability (P) that a gene tree has the same topology as that of the species tree. When one gene (allele) is used from each of the species involved, the probability can be expressed as a simple function of Ti = ti/(2N), where ti is the evolutionary time measured in generations for the ith internodal branch of the species tree and N is the effective population size. When any of the Ti's is less than 1, the probability P becomes considerably less than 1.0. This probability cannot be substantially increased by increasing the number of alleles sampled from a locus. To increase the probability, one has to use DNA sequences from many different loci that have evolved independently of each other.      

Taking a Comparative Approach: Analysing Personality as a Multivariate Behavioural Response across Species

Animal personality, repeatable behaviour through time and across contexts, is ecologically and evolutionarily important as it can account for the exhibition of sub-optimal behaviours. Interspecific comparisons have been suggested as important for understanding the evolution of animal personality; however, these are seldom accomplished due, in part, to the lack of statistical tools for quantifying differences and similarities in behaviour between groups of individuals. We used nine species of closely-related coral reef fishes to investigate the usefulness of ecological community analyses for the analysis of between-species behavioural differences and behavioural heterogeneity. We first documented behavioural carryover across species by observing the fishes' behaviour and measuring their response to a threatening stimulus to quantify boldness. Bold fish spent more time away from the reef and fed more than shy fish. We then used ecological community analysis tools (canonical variate analysis, multi-response permutation procedure, and permutational analysis of multivariate dispersion) and identified four 'clusters' of behaviourally similar fishes, and found that the species differ in the behavioural variation expressed; some species are more behaviourally heterogeneous than others. We found that ecological community analysis tools are easily and fruitfully applied to comparative studies of personality and encourage their use by future studies.     

Genetic variation over 10,000 years in Ctenomys: comparative phylochronology provides a temporal perspective on rarity, environmental change and demography

An understanding of how ecological traits influence past species response to environmental change can aid our future predictions of species persistence. We used ancient DNA and serial coalescent modelling in a hypothesis-testing framework to reveal differences in temporal genetic variation over 10,000 years for two species of subterranean rodents that currently differ in rarity (abundance, range size and habitat specificity) and mating system, but that reside in the same volcanically active region. Comparative phylochronologic analyses indicated little genetic change and suggest genetic stability in the solitary widespread Ctenomys haigi over thousands of years. In contrast, we found a pattern of haplotypic turnover in the rare and currently endangered Ctenomys sociabilis. Serial coalescent modelling indicated that the best-fit models of microevolutionary change included gene flow between isolated populations for this species. Although C. haigi and C. sociabilis are congeners that share many life history traits, they have behavioural, habitat-preference and population-size differences that may have resulted in contrasting patterns of temporal variation during periods of environmental change.     

A computational framework for the study of confidence in humans and animals

Confidence judgements, self-assessments about the quality of a subject's knowledge, are considered a central example of metacognition. Prima facie, introspection and self-report appear the only way to access the subjective sense of confidence or uncertainty. Contrary to this notion, overt behavioural measures can be used to study confidence judgements by animals trained in decision-making tasks with perceptual or mnemonic uncertainty. Here, we suggest that a computational approach can clarify the issues involved in interpreting these tasks and provide a much needed springboard for advancing the scientific understanding of confidence. We first review relevant theories of probabilistic inference and decision-making. We then critically discuss behavioural tasks employed to measure confidence in animals and show how quantitative models can help to constrain the computational strategies underlying confidence-reporting behaviours. In our view, post-decision wagering tasks with continuous measures of confidence appear to offer the best available metrics of confidence. Since behavioural reports alone provide a limited window into mechanism, we argue that progress calls for measuring the neural representations and identifying the computations underlying confidence reports. We present a case study using such a computational approach to study the neural correlates of decision confidence in rats. This work shows that confidence assessments may be considered higher order, but can be generated using elementary neural computations that are available to a wide range of species. Finally, we discuss the relationship of confidence judgements to the wider behavioural uses of confidence and uncertainty.     

Behavioural differences between two captive populations of red jungle fowl (Gallus gallus) with different genetic background,raised under identical conditions

Ex situ conservation of threatened species may lead to behavioural adaptation, which can affect success of reintroduction attempts. In previous studies, we investigated the effects of captivity on the behaviour of red jungle fowl (Gallus gallus) and found that captive populations differed behaviourally as well as genetically. The aim of the present study was to compare the behaviour of two of the previously studied populations, raised under identical conditions. Eggs were collected from birds at Copenhagen zoo (Cop) and Götala research station (Got) and were incubated and hatched together. Twenty-eight birds (16 Got and 12 Cop) were reared together and tested in eight different behavioural tests, measuring different aspects of fear-related behaviours as well as exploratory and social behaviours. The study revealed several differences in fear-related behaviours between the populations but none in exploratory or social behaviours. In general, one of the populations (Cop) showed more intense fear behaviours than the other (Got), which instead were less fearful in their behaviours. This indicates that breeding animals in captivity may lead to behavioural modifications, which can affect the outcome of reintroductions. The results further suggest that fear-related behaviours are dependent on the genetic background of the animals while social behaviours may be more influenced by the social environment. Since fear-related behaviours, such as predator avoidance and fear of humans, are essential for a life in the wild, these aspects are crucial for the breeding of animals in captivity for conservation purposes.     

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.     

The genetics of pathogen avoidance in Caenorhabditis elegans

Much attention is rightly focused on how microbes cause disease, but they can also affect other aspects of host physiology, including behaviour. Indeed, pathogen avoidance behaviours are seen across animal taxa and are probably of major importance in nature. Here, we review what is known about the molecular genetics underlying pathogen avoidance in the nematode Caenorhabditis elegans. In its natural environment, the soil, this animal feeds on microbes and is continuously exposed to a diverse mix of microorganisms. Nematodes that develop efficient behavioural responses that enhance their attraction to sources of food and avoidance of pathogens will have an evolutionary advantage. C. elegans can specifically detect natural products of bacteria, including surfactants (such as serrawettin) and acylated homoserine lactone autoinducers, and it can learn to avoid pathogenic species. To date, several distinct mechanisms have been shown to be involved in pathogen avoidance. They are based on G protein-like, insulin-like and neuronal serotonin signalling. We discuss recent findings on the mechanisms of pathogen recognition in C. elegans, the relationship between alternative behavioural defences and also between these and other life-history traits. We propose that the selective pressure associated with avoidance behaviours influence both pathogen and host evolution.