
Genes and Behaviour
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The great debate of nature versus nurture rages on -- but our understanding of the genetic basis of many behaviors has expanded over the last decade, and there is now very good evidence showing that seemingly complex behaviours can have relatively simple genetic underpinnings, but also that most behaviours have very complicated genetic and environmental architecture. Studies have also clearly shown that behaviors, and other traits, are influenced not just by genes and the environment, but also by the statistical interaction between the two. This book aims to end the nature versus nurture argument by showing that behaviors are nature and nurture and the interaction between the two, and by illustrating how single genes can explain some of the variation in behaviors even when they are seemingly complex.
Genes and Behaviour: Beyond Nature-Nurture puts to rest the nature versus nurture dichotomy, providing an up-to-date synopsis of where we are, how far we've come and where we are headed. It considers the effects of a dual-inheritance of genes and culture, and genes and social environment, and highlights how indirect genetic effects can affect the evolution of behavior. It also examines the effect of non-self genes on the behavior of hosts, shines a light on the nature and nurturing of animal minds and invites us to embrace all the complexity nature and nurture generates, and more.
* Explores exciting new findings about behavior and where we go from here
* Features contributions by top scholars of the subject
* Seeks to end the nature versus nurture debate forever
Genes and Behaviour: Beyond Nature-Nurture is a unique, and eye-opening read that will appeal to Ph.D. Students, post-doctoral fellows, and researchers in evolution and behavior. Additionally, the book will also be of interest to geneticists, sociologists and philosophers.
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Persons
David J. Hosken, PhD, is Professor of Evolutionary Biology at the Centre for Ecology & Conservation, University of Exeter, Cornwall, Penryn, UK.
John Hunt, PhD, is Professor of Ecology at the Centre for Ecology & Conservation, University of Exeter, Cornwall, Penryn, UK and at the School of Science & Health, Hawkesbury Institute for the Environment, Western Sydney University, Hawkesbury, NSW, Australia.
Nina Wedell, PhD, is a Professor of Evolutionary Biology at the Centre for Ecology & Conservation, University of Exeter, Cornwall, Penryn, UK.
Content
List of Contributors xiii
Preface xv
1 Nature, Nurture, and Nature-by-Nurture - Killing the Dichotomy 1
David J. Hosken, John Hunt and Nina Wedell
Acknowledgements 7
References 7
2 Ultimate (Re)Thinking for Behavioural Biology 11
Sasha R. X. Dall, John M. McNamara and Alastair J. Wilson
2.1 Evolutionary Reasoning in Modern Behavioural Biology 13
2.2 A Quantitative Genetic View of Behavioural Evolution 15
2.3 Short-Term Ultimate Reasoning: Behavioural Genetics in a Functional Context 20
2.4 Concluding Remarks 21
References 22
3 How the Dual Inheritance of Genes and Culture Shapes Behaviour: A Critical Review with a Focus on Human Culture and Behavioural Diversity 27
Thomas E. Currie
3.1 Culture and Behaviour 27
3.2 Cultural Evolution 30
3.2.1 Processes of Cultural Evolution 31
3.2.1.1 Variation 31
3.2.1.2 Inheritance 32
3.2.1.3 Selection and Fitness 34
3.3 Insights from Cultural Evolutionary Approaches 37
3.3.1 Adaptive and Maladaptive Behaviour 37
3.4 Cultural History 39
3.5 Culture and the Evolution of Co-operation 42
3.6 Gene-Culture Coevolution 45
3.7 Conclusion 48
Acknowledgements 50
References 50
4 Beyond Genes and Environments: Indirect Genetic Effects and the Evolution of Behaviour 61
John Hunt, James Rapkin, Clarissa M. House and Alastair J. Wilson
4.1 A Quantitative Genetic View of Behavioural Evolution without IGEs 63
4.2 Adding IGEs to the Traditional Theory 66
4.2.1 'Trait-Based' and 'Variance Partitioning' Models of IGEs 67
4.3 From Theory Towards Empiricism 68
4.3.1 Using Trait-Based Models 69
4.3.2 Using Variance Partitioning Models 71
4.3.3 Is Knowledge of the Interactor Trait Critical to Your Study? 72
4.4 Empirical Evidence for IGEs on Behavioural Traits 73
4.4.1 Social Plasticity of Behaviour is Widespread 73
4.4.2 Does Social Plasticity Generate IGEs on Focal Behaviour? 78
4.5 What are the Evolutionary Consequences of IGEs? 81
4.5.1 What about the Role of Social Selection? 82
4.5.2 What Happens When ¿ is Also Able to Evolve? 83
4.5.3 Can IGEs Influence Other Important Evolutionary Processes? 83
4.5.4 What are the Longer Term Consequences of IGEs? 85
4.6 Conclusions and Future Directions 85
References 87
5 Genes and Behaviour 93
Chelsea A. Weitekamp and Laurent Keller
5.1 Genetic Architecture of Phenotypic Traits 94
5.2 Effects of Single Genes on Behaviour 95
5.2.1 The Foraging Gene and Food-Search Behaviour 97
5.2.2 Arginine Vasopressin Receptor and Pair-Bonding Behaviour 98
5.2.3 Neuropeptide Y Homolog, Sensory Neurons, and Social Feeding Behaviour 98
5.3 Effects of Supergenes on Behaviour 99
5.3.1 Social Organization in Ants 100
5.3.2 Alternative Mating Tactics in Birds 100
5.4 Evolvability of Behaviour-Associated Genes 101
5.5 Are Behavioural Traits Unique? 101
5.6 Conclusion 103
Acknowledgements 103
References 103
6 Genes and Environments in Drosophila Sex 111
David J. Hosken, Amanda Bretman, Stephen F. Goodwin and C. Ruth Archer
6.1 Some Challenges 111
6.2 Introducing Drosophila 112
6.3 The Behaviours 112
6.4 The Genes 113
6.4.1 Single Genes 113
6.4.2 Many Additive Genes 115
6.5 The Environments and the Interactions 116
6.5.1 Social Environments 116
6.5.2 Abiotic Environments 119
6.6 Conclusions 120
Acknowledgements 120
References 120
7 Nature and Nurture in Parental Care 131
Nick J. Royle and Allen J. Moore
7.1 Genetics Underlying Parental Care 133
7.1.1 Quantitative Genetic Studies 134
7.1.2 Molecular Genetic Studies 135
7.2 Parental Care is Environmentally Sensitive 137
7.2.1 Hormonal Mediation of Parental Care 138
7.3 Gene by Family Environment Interactions 141
7.3.1 GxFE Studies 141
7.3.2 Heritability of the Social Environment and IGEs 143
7.3.3 Coadaptation and Correlational Selection (Social Epistasis as a Special Case of GxFE) 145
7.4 Summary and Conclusion 147
References 148
8 The Effect of Non-Self Genes on the Behaviour of Hosts 157
Nina Wedell
8.1 What are Non-Self Genes (NSGs)? 158
8.2 Indirect Effects of NSGs 158
8.3 Direct Effects of NSGs 159
8.4 Host Responses 160
8.5 Odour is a Key Signal 161
8.6 Kin Recognition 162
8.7 Mate Choice and Reproductive Behaviour 163
8.8 Aggressiveness 166
8.9 Activity, Aggregation, and Dispersal 167
8.10 Feeding 168
8.11 Learning and Memory 170
8.12 Summary and Conclusion 171
References 172
9 The Nature and Nurturing of Animal Minds 181
Alex Thornton and Neeltje J. Boogert
9.1 Cognition Evolves 183
9.1.1 Adaptive Cognitive Specializations 183
9.1.2 Heritability of Cognitive Traits 185
9.2 Cognition Develops 187
9.2.1 Cognitive Consequences of a Poor Start in Life 187
9.2.2 Cognitive Silver Spoons 188
9.2.3 Adaptive Developmental Plasticity in Cognition 189
9.3 Cognitive Reaction Norms: Mind-Moulding Gene-by-Environment Interactions 191
9.3.1 The Mystery of (the Lack of) Cognitive Resilience 192
9.3.2 Practice Makes Perfect: Genetic Quality and Cognitive Silver Spoons 193
9.3.3 Cultural and Epigenetic Inheritance of Cognitive Traits 194
9.3.4 Gene by Environment and Methodological Issues in Comparative Cognition 194
9.4 Conclusion 195
References 196
10 Evolution and Human Behaviour: Helping to Make Sense of Modern Life 203
Louise Barrett and Gert Stulp
10.1 Understanding Interaction 204
10.2 Understanding the Scope and Limits of an Evolutionary Approach 205
10.3 Evolutionary Thinking as Puzzle Solving 206
10.4 Recognizing the Consequences of Our Actions 208
10.5 Thinking Differently about Fertility Control 210
10.6 Modern Contraception and Mate Choice 212
10.7 Evolution and Assisted Reproductive Technologies 214
10.8 No Free Lunch 216
10.9 Conclusion 217
References 218
11 Next-Gen and the Study of Behaviour 223
Simone Immler
11.1 Current Sequencing Technologies 223
11.1.1 Genome-Wide Association Study (GWAS) and Linkage Mapping 224
11.1.1.1 Microarrays 226
11.1.1.2 RAD Sequencing 227
11.1.1.3 Exome Sequencing 227
11.1.1.4 Whole-Genome Sequencing 227
11.1.2 Gene Expression Analyses 228
11.1.2.1 RNA Sequencing (RNAseq) 228
11.1.3 Epigenetic Analyses 228
11.1.3.1 CHiP Sequencing (CHiPseq) 228
11.1.3.2 Bisulfite Sequencing 229
11.2 Caveats and Challenges and Some Solutions 229
11.2.1 Solid Phenotype 229
11.2.2 Sample Quality 230
11.2.3 Sampling 230
11.2.4 Libraries and Sample Pools 230
11.2.5 Reference Genome 231
11.2.6 Sample Size 232
11.2.7 Replication 232
11.2.8 Coverage 232
11.2.9 Pilot Studies 233
11.2.10 Time and Planning 233
11.2.11 Bioinformatics 233
11.2.12 Collaboration 234
11.3 Linking Behavioural Phenotypes to Genotypes using NGS 234
11.4 What's Next 237
11.4.1 Understanding the Non-Coding Regions of the Genome 238
11.4.2 Gene Knock-down and Knock-out in Non-Model Organisms 238
11.5 Concluding Remarks 240
References 240
12 Nature-Nurture in the Twenty-First Century 245
Nina Wedell, John Hunt and David J. Hosken
Acknowledgements 249
References 249
Index 253
1
Nature, Nurture, and Nature-by-Nurture - Killing the Dichotomy
David J. Hosken1, John Hunt1,2 and Nina Wedell1
1 Centre for Ecology & Conservation, University of Exeter, Penryn Campus, Penryn, TR10 9EZ, UK
2 School of Science and Health & Hawkesbury Institute for the Environment, Western Sydney University, Hawkesbury, NSW 2793, Australia
The primary purpose of this book is to provide a broad snapshot of recent findings showing how the environment and genes influence behaviour. At face value, this should be uncontroversial but unfortunately, the history of genetics includes eugenic movements and Lysenkoism. As a result, discussions of how nature and nurture affect behaviour have been dogged by polemic disputes because ideological views about their contributions have tended to cloud what is really an empirical question. This is in some ways exemplified by the book Not in Our Genes (Lewontin et al. 1984), which begins with a political confession from the authors - we are committed socialists - and starts with a chapter on right-wing politics and determinism. For us, the evidence, and not political or any other beliefs, is what counts and any 'belief' approach puts the desire for the world to be a certain way ahead of the evidence that it is not so, ultimately committing a version of the naturalistic fallacy - if something is 'natural', it is morally correct, which is clearly rubbish (also see Chapter 10). Infanticide, cannibalism, forced copulation (rape), and killing other members of your species (murder) are rife in nature, but it would be difficult to convince anyone of intelligence that these acts are moral because they are natural. Furthermore, 'politically' motivated arguments against 'reductionism', reducing complex behaviours to single causes, are frequently concocted to protect against a biological determinism that must be fought at all costs. However, as we hope to explain, acknowledging that there are genes underlying behaviour, even genes of large effect, is imperative if that is what the data tell us. After all, it is no use playing music to cows if milk yield is totally determined by genes and unaffected by the environment, and as we outline below, in a polygenic world that includes inevitable environmental effects and all manner of interactions, prediction is tricky and determinism dubious because of the probabilistic and complex nature of the gene-behaviour link. But again, even if single genes were completely responsible for single behaviours, which they cannot be in the strictest sense (see below), let us not fall into a naturalistic fallacy.
Rather than engage in further fruitless arguments about world-views, this book explores exciting new findings about behaviour and where we go from here. Before moving on to these new advances and the interesting questions that arise from them, we wish to make another - a final? - attempt to kill the nature versus nurture polarity that has plagued the study of behaviour. This dichotomy is largely, but not totally, dead in academic circles but still haunts many debates outside academia, from views on teaching and punishment to politics and the media more generally. It potentially has grave consequences and is a serious distraction to the much more fruitful and interesting discussion about the determinants and influences of behaviour.
Most behaviours, like any aspect of the phenotype, are not influenced by either nature or nurture but by both and by the statistical interaction between nature and nurture (see reviews in Boake 1994; Sokolowski 2001; Bucan and Abel 2002; van Oers et al. 2005; Hunt and Hosken 2014; Anholt and Mackay 2015) (see also Chapters 6, and 7). To explain, starting with the genetic effects, behaviours (and other characters, for that matter) are typically polygenic (Anholt and Mackay 2004). That is, they have complicated genetic architecture that involves many segregating genes with pleiotropic effects and are characterized by complicated epistatic interactions (Anholt and Mackay 2004). In other words, there are lots of genes, each can affect many characters, and the effects of any one gene frequently depend on the other genes it is associated with. There are exceptions to some of this (see Chapter 05), with, for example, foraging movement in Drosophila melanogaster having two distinct behavioural phenotypes that are largely determined by a single gene (reviewed in Sokolowski 2001), and aggression being altered by transposon upregulation of a cytochrome P450 gene (Rostant et al. 2017). However, even these large single-gene effects can be complicated by epistasis (gene-gene interactions) (e.g. Smith et al. 2011; Rostant et al. 2015).
Nonetheless, most behaviours are influenced by many genes, often of small effect, and because of this, we may never uncover all the precise genes that influence a behavioural phenotype. As a result, a statistical approach is needed to describe the average effects of genes on a behaviour and, importantly, to show how genes affect the variation around the mean. The distinction between an average effect and the variation around it is crucial, because for the most part there is not a single gene for phenotype A or B; rather, there are many genes that alter the probability of expressing phenotype A or B. Thus, many interesting traits do not vary discretely but are continuous (Falconer 1981; Roff 1997; Lynch and Walsh 1998), and genes influence the likelihood that an individual will express more or less of the trait in question.
The simplest statistical approach to understanding these relationships involves partitioning the variation in the behaviour of interest into the sum of the genetic effects and the variance unexplained is then due to the environment (which includes maternal/paternal effects, indirect genetic effects, ecology and abiotic factors like temperature, food, and water), or alternatively, testing a range of genotypes across environments and then partitioning effects into genes, environment, and their interaction (how genes and environment affect each other to determine phenotypic variation) (see Chapter 04). This reveals exactly how genes, the environment, and their interaction can affect phenotypes, including behavioural phenotypes.
Figure 1.1 A pictorial explanation of genotype-by-environment interactions (GxE). In (a) we show a plant GxE - for simplicity's sake (see explanation below) - and in (b) cricket calling behaviour as a hypothetical behavioural example. (a) Three plant genotypes (clones) grown in two environments that only differ in how much water each plant receives, but everything else about the environments is identical. This means that each plant experiences exactly the same conditions within each environment and differences in water between environments. Therefore, plant size differences within each environment are due to just the genetic differences between plants. However, because each plant genotype is found in each environment, any difference in the average plant phenotype across environment is due to the environmental (water) differences alone. The changes in relative size across environments (i.e. Clone 1 is biggest in Environment 1, but smallest in Environment 2) represents a genotype-by-environment interaction. So plant size variation is due to genetic differences, environmental differences and an interaction between the genetic and environmental differences. The same principles apply to any phenotype, including behaviour. (b) This figure shows the same interaction-type across cricket calls where the sonograms above and below the cricket images show the hypothetical songs females of each hypothetical genotype are most attracted to across two imaginary environments. In Environment 1, call rates are slower than in Environment 2 (there is an environmental effect on preferred calls), and each genotype prefers different calls (a genetic effect), but the type of call preferred depends on the environment sampled (gene-by-environment effect).
To use a simple morphological example to make this point very clearly while noting the principles are exactly the same for behaviour: if we could take three plant-clones (three distinct plant genotypes (Figure 1.1) and grow each of them in two highly controlled environments that only differed from each other by how much water was available and all else was exactly the same, then the differences in plant heights within each environment would be due to just the genes, and the average difference in heights between environments would be due to environmental differences alone. And if the effects of the genes on the phenotype varied across the two environments (i.e. the biggest genotype in environment 1 is the smallest in environment 2), then we have a genotype-by-environment interaction (we additionally include a hypothetical behavioural example as well; see Figure 1.1). To put that into the simplest terms:
(1.1)where P = the phenotype, G = the genotype, E = the environment, and GxE = the interaction between genotype and environment, and this is as true of behaviour as it is of morphology. And if we are talking about variation around average behaviours, then we have:
(1.2)where VP = phenotypic variation, VG = genetic variation...
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