Evolutionary Causes Research Articles

NATURAL HISTORY FIRST (BUT DON'T STOP THERE)

This quote from Agassiz welcomes visitors to the main entrance of the Ruthven Museums Building at the University of Michigan, beseeching them to collect their own data and draw their own conclusions. The sentiment has inspired generations of evolutionary biologists, who continue the long tradition of deductive science epitomized by Darwin and Wallace. The fundamental questions about evolution have always been borne from direct observation of, and curiosity about, nature. In the best cases, the process leads to elegant tests of hypotheses and formulations of general theories. No practitioners of this art of investigation have done it with more rigor, provided deeper insight, or better illuminated the aesthetic qualities of science, than Peter and Rosemary Grant. It is fitting, then, that the careers of the Grants (while showing no signs of ebbing toward a twilight!) should be celebrated by assembling a fine cadre of scientific naturalists to share their own observations and deductions. In Search of the Causes of Evolution is a collection of essays based on presentations at a symposium organized by Princeton University on the occasion of the Grants’ official “retirement.” The chapters are remarkably true to the theme that observation leads the way to detailed dissections of the underlying mechanisms of evolution. The author list represents some of the most significant contributors at the forefront of evolutionary research. Although readers will recognize most of the study systems (e.g., anoles, beach mice, dung beetles, sticklebacks even make two appearances), the authors generally have done an admirable job of resisting the temptation to rehash old work and have contributed new data or syntheses to the volume. The resultant book thereby serves as a low-altitude reconnaissance flight over some of the most exciting current research in evolutionary ecology. The ground covered by the essays is extensive, as it should be under a title purporting to encompass the causes of evolution. As anyone who has taught an introductory evolution course can attest, the scope of topics that we seek to explain is staggering. One person’s bread and butter might not even be included on another’s list. The Grants have at least attempted to span this space by including chapters across the spectrum from the evolution of early earth environments (Andrew Knoll and David Johnston) and macroevolutionary patterns of diversification (David Jablonski) to the search for “behavior genes” (Hopi Hoekstra) and the population genetics of island endemism (Trevor Price and colleagues). True to the tradition of the Grants’ own work, however, the majority of essays emphasizes the interplay of selection and genetics as drivers of biodiversity. This is a collection that is unapologetically adaptationist in its perspective on evolutionary mechanisms. So what do we learn about where the grander field of evolutionary biology is headed when we collect marquis names with license to write about whatever they want? First, evolutionary research is not dominated by traditional model systems. Indeed,

Evolutionary causes and consequences of sequential polyandry in anuran amphibians

Among anuran amphibians (frogs and toads), there are two types of polyandry: simultaneous polyandry, where sperm from multiple males compete to fertilize eggs, and sequential polyandry, where eggs from a single female are fertilized by multiple males in a series of temporally separate mating events, and sperm competition is absent. Here we review the occurrence of sequential polyandry in anuran amphibians, outline theoretical explanations for the evolution of this mating system and discuss potential evolutionary implications. Sequential polyandry has been reported in a limited number of anurans, but its widespread taxonomic and geographic distribution suggests it may be common. There have been no empirical studies that have explicitly investigated the evolutionary consequences of sequential polyandry in anurans, but species with this mating pattern share an array of behavioural, morphological and physiological characteristics, suggesting that there has been common sexual selection on their reproductive system. Sequential polyandry may have a number of adaptive benefits, including spreading the risk of brood failure in unpredictable environments, insuring against male infertility, or providing genetic benefits, either through good genes, intrinsic compatibility or genetic diversity effects. Anurans with sequential polyandry provide untapped opportunities for innovative research approaches that will contribute significantly to understanding anuran evolution and also, more broadly, to the development of sexual-selection and life-history theory.

Variation in personality and behavioural plasticity across four populations of the great tit Parus major

1. Interest in the evolutionary origin and maintenance of individual behavioural variation and behavioural plasticity has increased in recent years. 2. Consistent individual behavioural differences imply limited behavioural plasticity, but the proximate causes and wider consequences of this potential constraint remain poorly understood. To date, few attempts have been made to explore whether individual variation in behavioural plasticity exists, either within or between populations. 3. We assayed 'exploration behaviour' among wild-caught individual great tits Parus major when exposed to a novel environment room in four populations across Europe. We quantified levels of individual variation within and between populations in average behaviour, and in behavioural plasticity with respect to (i) repeated exposure to the room (test sequence), (ii) the time of year in which the assays were conducted and (iii) the interval between successive tests, all of which indicate habituation to novelty and are therefore of functional significance. 4. Consistent individual differences ('I') in behaviour were present in all populations; repeatability (range: 0.34-0.42) did not vary between populations. Exploration behaviour was also plastic, increasing with test sequence - but less so when the interval between subsequent tests was relatively large - and time of year; populations differed in the magnitude of plasticity with respect to time of year and test interval. Finally, the between-individual variance in exploration behaviour increased significantly from first to repeat tests in all populations. Individuals with high initial scores showed greater increases in exploration score than individuals with low initial scores; individual by environment interaction ('I × E') with respect to test sequence did not vary between populations. 5. Our findings imply that individual variation in both average level of behaviour and behavioural plasticity may generally characterize wild great tit populations and may largely be shaped by mechanisms acting within populations. Experimental approaches are now needed to confirm that individual differences in behavioural plasticity (habituation) - not other hidden biological factors - caused the observed patterns of I × E. Establishing the evolutionary causes and consequences of this variation in habituation to novelty constitutes an exciting future challenge.

In search of the causes of evolution: from field observations to mechanisms

List of Contributors ix Preface xi Introduction to Section I: The Origins of Biological Diversity 1 Chapter One: The Big Picture: A Tripartite View of Life and Environments through Time by Andrew H. Knoll and David T. Johnston 5 Chapter Two: Macroevolutionary Trends in Time and Space by David Jablonski 25 Chapter Three: Dinosaurs Live! 4 by Philip J. Currie 4 Chapter Four: Phylogeography and Phylogenetics in the Nuclear Age by Christopher N. Balakrishnan, June Y. Lee, and Scott V. Edwards 65 Introduction to Section II: Mechanisms, Molecules, and Evo-Devo 89 Chapter Five: The Flexibility of Butterfly Wing Color Patterns and Evolution in Morphospace by Paul M. Brakefield and Mathieu Joron 93 Chapter Six: Genetics, Geology, and Miracles by David Kingsley 115 Chapter Seven: Evolutionary Genetics of Pigmentation Loss in the Blind Mexican Cavefish by Joshua B. Gross and Clifford J. Tabin 131 Chapter Eight: A Developmental View of Exaggerated Growth and Conditional Expression in the Weapons of Sexual Selection by Douglas J. Emlen 149 Introduction to Section III: Morphology and Behavior 173 Chapter Nine: How Does Morphology Affect Performance in Variable Environments? By Mimi A. R. Koehl 177 Chapter Ten: In Search of the Elusive Behavior Gene by Hopi E. Hoekstra 192 Chapter Eleven: There Must Be Finches--Charles Darwin, Prickly Pears, and Pollination Biology by May R. Berenbaum 211 Chapter Twelve: The Adaptive Radiation of Coevolving Prodoxid Moths and Their Host Plants: Greya Moths and Yucca Moths by John N. Thompson 228 Introduction to Section IV: Ecological Diversity 247 Chapter Thirteen: Ecological and Geographical Influences on the Allopatric Phase of Island Speciation by Trevor Price, Albert B. Phillimore, Myra Awodey, and Richard Hudson 251 Chapter Fourteen: Geographical Mode and Evolutionary Mechanism of Ecological Speciation in Cichlid Fish by Ole Seehausen and Isabel Santos Magalhaes 282 Chapter Fifteen: A Tale of Two Radiations: Similarities and Differences in the Evolutionary Diversification of Darwin's Finches and Greater Antillean Anolis Lizards by Jonathan B. Losos 309 Chapter Sixteen: Clarifying the Mechanisms of Evolution in Sticklebacks Using Field Studies of Natural Selection on Genes by Rowan D. H. Barrett and Dolph Schluter 332 Chapter Seventeen: The Book and the Future: Perspective and Prospective by Peter R. Grant and B. Rosemary Grant 347 Chapter Eighteen: A Festival for Rosemary and Peter Grant by David B. Wake 360 Index 367

Oxidative lipid, protein, and DNA damage as oxidative stress markers in vascular complications of diabetes mellitus

The purpose of this study was to determine the effects of diabetic complications on oxidation of proteins, lipids, and DNA and to investigate the relationship between oxidative damage markers and clinical parameters. The study group consisted of 69 type 2 diabetic patients (20 patients without complication, 49 patients with complication) who attended internal medicine outpatient clinics of Istanbul Education and Research Hospital and 19 healthy control subjects. In serum samples of both diabetic patients and healthy subjects, 8-hydroxy-2'deoxyguanosine (8-OHdG), as a marker of oxidative DNA damage, N(ε)-(hexanoyl)lysine (HEL) and 15-F2t-iso-prostaglandin (15-F2t-IsoP). as products of lipooxidative damage, advanced oxidation protein products (AOPP), as markers of protein damage, and paraoxonase1 (PON1) as antioxidant were studied. 15-F2t-IsoP (p < 0.005) and AOPP (p < 0.001) levels were significantly higher in diabetic group than control group while there were no significant differences in levels of 8-OHdG and HEL between the two groups. AOPP (p < 0.001) and 8-OHdG (p < 0.001) were significantly higher in diabetic group with complications compared to diabetic group without complications. Increased formation of free radicals and oxidative stress, under conditions of hyperglycaemia, is one of the probable causes for evolution of complications in diabetes mellitus. Our study supports the hypothesis that oxidant/antioxidant balance is disturbed in diabetic patients.

Natural levels of polyandry: differential sperm storage and temporal changes in sperm competition intensity in wild yellow dung flies

Summary 1. Polyandry is common in insects. Nevertheless, the evolutionary causes and consequences of this phenomenon remain contentious, in part because of a lack of information about natural mating rates and the fact that most post-copulatory processes are hidden from view within female reproductive tracts. 2. We captured wild female yellow dung flies (Scathophaga stercoraria) over the whole spring season and genotyped the sperm from their spermathecae to obtain information on sperm transfer, sperm storage and natural levels of polyandry for this model species of post-copulatory sexual selection research. 3. On average, females stored sperm from a minimum of 2·47 males (based on the most conservative estimate). Incorporating knowledge of population allele frequencies yielded a slightly higher estimate of 3·33 mates per female. 4. Sperm storage and therefore sperm competition intensity showed high temporal variation. The proportion of multiply mated females (i.e. females with sperm from ≥2 males within their sperm stores) and the absolute number of ejaculates detected within females increased strongly over the spring season before sharply decreasing as midsummer approached. 5. Interestingly, we detected a positive relationship between the number of stored ejaculates and females’ wing injuries, suggesting that mating not only causes measurable cumulative damage to wild females but also provides a potential mechanism by which males may be able to assess the intensity of sperm competition within a female. 6. Our study found no evidence for intraejaculate sperm sorting, but importantly, the number of ejaculates in storage differed amongst the three sperm storage organs (spermathecae) of female yellow dung flies. Different sperm mixtures across the spermathecae could enable females to bias paternity towards certain males if females can selectively use sperm from a certain spermatheca at the time of fertilization.

Female competition and its evolutionary consequences in mammals

Following Darwin's original insights regarding sexual selection, studies of intrasexual competition have mainly focused on male competition for mates; by contrast, female reproductive competition has received less attention. Here, we review evidence that female mammals compete for both resources and mates in order to secure reproductive benefits. We describe how females compete for resources such as food, nest sites, and protection by means of dominance relationships, territoriality and inter-group aggression, and by inhibiting the reproduction of other females. We also describe evidence that female mammals compete for mates and consider the ultimate causes of such behaviour, including competition for access to resources provided by mates, sperm limitation and prevention of future resource competition. Our review reveals female competition to be a potentially widespread and significant evolutionary selection pressure among mammals, particularly competition for resources among social species for which most evidence is currently available. We report that female competition is associated with many diverse adaptations, from overtly aggressive behaviour, weaponry, and conspicuous sexual signals to subtle and often complex social behaviour involving olfactory signalling, alliance formation, altruism and spite, and even cases where individuals appear to inhibit their own reproduction. Overall, despite some obvious parallels with male phenotypic traits favoured under sexual selection, it appears that fundamental differences in the reproductive strategies of the sexes (ultimately related to parental investment) commonly lead to contrasting competitive goals and adaptations. Because female adaptations for intrasexual competition are often less conspicuous than those of males, they are generally more challenging to study. In particular, since females often employ competitive strategies that directly influence not only the number but also the quality (survival and reproductive success) of their own offspring, as well as the relative reproductive success of others, a multigenerational view ideally is required to quantify the full extent of variation in female fitness resulting from intrasexual competition. Nonetheless, current evidence indicates that the reproductive success of female mammals can also be highly variable over shorter time scales, with significant reproductive skew related to competitive ability. Whether we choose to describe the outcome of female reproductive competition (competition for mates, for mates controlling resources, or for resources per se) as sexual selection depends on how sexual selection is defined. Considering sexual selection strictly as resulting from differential mating or fertilisation success, the role of female competition for the sperm of preferred (or competitively successful) males appears particularly worthy of more detailed investigation. Broader definitions of sexual selection have recently been proposed to encompass the impact on reproduction of competition for resources other than mates. Although the merits of such definitions are a matter of ongoing debate, our review highlights that understanding the evolutionary causes and consequences of female reproductive competition indeed requires a broader perspective than has traditionally been assumed. We conclude that future research in this field offers much exciting potential to address new and fundamentally important questions relating to social and mating-system evolution.

SEX RATIO EVOLUTION UNDER PROBABILISTIC SEX DETERMINATION

Sex allocation theory has been remarkably successful at explaining the prevalence of even sex ratios in natural populations and at identifying specific conditions that can result in biased sex ratios. Much of this theory focuses on parental sex determination (SD) strategies. Here, we consider instead the evolutionary causes and consequences of mixed offspring SD strategies, in which the genotype of an individual determines not its sex, but the probability of developing one of multiple sexes. We find that alleles specifying mixed offspring SD strategies can generally outcompete alleles that specify pure strategies, but generate constraints that may prevent a population from reaching an even sex ratio. We use our model to analyze sex ratios in natural populations of Tetrahymena thermophila, a ciliate with seven sexes determined by mixed SD alleles. We show that probabilistic SD is sufficient to account for the occurrence of skewed sex ratios in natural populations of T. thermophila, provided that their effective population sizes are small. Our results highlight the importance of genetic drift in sex ratio evolution and suggest that mixed offspring SD strategies should be more common than currently thought.

The future of plant–pollinator diversity: Understanding interaction networks across time, space, and global change

Structural analysis of plant-pollinator networks has revealed remarkably high species and interaction diversity and highlighted the species important for pollination services. Although techniques to analyze plant-pollinator networks began to emerge a decade ago, the characterization of spatiotemporal variation of interactions is still in its infancy. Understanding the ecological and evolutionary causes and consequences of spatial and temporal variation in plant-pollinator interactions is important for both basic and applied questions in community structure and function, the evolution of floral traits, and the development of optimal conservation strategies. Here we review observational, theoretical, and experimental studies of temporal and spatial variation in plant-pollinator interaction networks to establish a foundation for future studies to incorporate perspectives in spatiotemporal variation. Such perspectives are crucial given the rapid environmental changes associated with habitat loss, climate change, and biological invasions, which we discuss in this context. The inherent plasticity of plant-pollinator interactions and network structure suggests that many species should be able to persist by responding to environmental changes quickly, even though the identity of their mutualistic partners may change.

Testing evolutionary hypotheses about the phylotypic period of zebrafish

Vertebrate embryos pass through a period of morphological similarity, the phylotypic period. Since Haeckel's biogenetic law of recapitulation, proximate and ultimate evolutionary causes of such similarity of embryos were discussed. We test predictions about changes in phenotypic and genetic variances that were derived from three hypotheses about the evolutionary origin of the phylotypic stage, i.e. random, epigenetic effects, and stabilizing selection. The random hypothesis predicts increasing values for phenotypic variances and stable or increasing values for genetic variances; the epigenetic effects hypothesis predicts declining values for phenotypic variances but stable or increasing values of genetic variances, and the stabilizing selection predicts stable phenotypic variances but decreasing genetic variances. We studied zebrafish as a model species, because it can be bred in large numbers as necessary for a quantitative genetics breeding design. A half-sib breeding scheme provided estimates of additive genetic variances from 11 embryonic characters from 12 through to 24 hr after fertilization, i.e. before, during (15-19 hr), and after the phylotypic period. Because additive genetic variances are size dependent, we calculated narrow-sense heritabilities as a size independent gauge of genetic contributions to the phenotype. The results show declining phenotypic variances and stable heritabilities. In conclusion, we reject the random and the stabilizing selection hypotheses and favor ideas about epigenetic effects that constrain the early embryonic development. Additive genetic variance during the phylotypic stage makes it accessible for evolution, thus explaining in a simple and straightforward way why the phylotypic period differs among vertebrates in timing, duration, and morphologies.

Extraordinary Sequence Divergence at Tsga8, an X-linked Gene Involved in Mouse Spermiogenesis

The X chromosome plays an important role in both adaptive evolution and speciation. We used a molecular evolutionary screen of X-linked genes potentially involved in reproductive isolation in mice to identify putative targets of recurrent positive selection. We then sequenced five very rapidly evolving genes within and between several closely related species of mice in the genus Mus. All five genes were involved in male reproduction and four of the genes showed evidence of recurrent positive selection. The most remarkable evolutionary patterns were found at Testis-specific gene a8 (Tsga8), a spermatogenesis-specific gene expressed during postmeiotic chromatin condensation and nuclear transformation. Tsga8 was characterized by extremely high levels of insertion-deletion variation of an alanine-rich repetitive motif in natural populations of Mus domesticus and M. musculus, differing in length from the reference mouse genome by up to 89 amino acids (27% of the total protein length). This population-level variation was coupled with striking divergence in protein sequence and length between closely related mouse species. Although no clear orthologs had previously been described for Tsga8 in other mammalian species, we have identified a highly divergent hypothetical gene on the rat X chromosome that shares clear orthology with the 5' and 3' ends of Tsga8. Further inspection of this ortholog verified that it is expressed in rat testis and shares remarkable similarity with mouse Tsga8 across several general features of the protein sequence despite no conservation of nucleotide sequence across over 60% of the rat-coding domain. Overall, Tsga8 appears to be one of the most rapidly evolving genes to have been described in rodents. We discuss the potential evolutionary causes and functional implications of this extraordinary divergence and the possible contribution of Tsga8 and the other four genes we examined to reproductive isolation in mice.

Rapid diversification and not clade age explains high diversity in neotropical Adelpha butterflies.

Latitudinal gradients in species richness are among the most well-known biogeographic patterns in nature, and yet there remains much debate and little consensus over the ecological and evolutionary causes of these gradients. Here, we evaluated whether two prominent alternative hypotheses (namely differences in diversification rate or clade age) could account for the latitudinal diversity gradient in one of the most speciose neotropical butterfly genera (Adelpha) and its close relatives. We generated a multilocus phylogeny of a diverse group of butterflies in the containing tribe Limenitidini, which has both temperate and tropical representatives. Our results suggest there is no relationship between clade age and species richness that could account for the diversity gradient, but that instead it could be explained by a significantly higher diversification rate within the predominantly tropical genus Adelpha. An apparent early larval host-plant shift to Rubiaceae and other plant families suggests that the availability of new potential host plants probably contributed to an increase in diversification of Adelpha in the lowland Neotropics. Collectively, our results support the hypothesis that the equatorial peak in species richness observed within Adelpha is the result of increased diversification rate in the last 10-15 Myr rather than a function of clade age, perhaps reflecting adaptive divergence in response to the dramatic host-plant diversity found within neotropical ecosystems.

Testing the molecular and evolutionary causes of a ‘leapfrog’ pattern of geographical variation in coloration

Understanding the mechanisms accounting for the evolution of phenotypic diversity is central to evolutionary biology. We use molecular and phenotypic data to test hypotheses for 'leapfrog' patterns of geographical variation, in which phenotypically similar, disjunct populations are separated by distinct populations of the same species. Phylogenetic reconstructions revealed independent evolution of melanic plumage characters in different populations in the Neotropical avian genus Arremon. Thus, phenotypic similarities between distant populations cannot be explained by close phylogenetic affinity. Nor can they be attributed to recurring mutations in the MC1R gene, a locus involved in melanic pigmentation. A coalescent analysis indicates that plumage traits have become fixed at a faster rate than expected under genetic drift, suggesting that selection underlies their repeated evolution. In contrast to views that genetic drift drives phenotypic differentiation in Neotropical montane birds, our results imply that geographical variation preceding speciation may reflect the action of deterministic selective processes.

Seeing the forest through the gene‐trees

The human genome is a dense forest of biological information for us to find our way through. In the past, we could view it as a forest, comfortably assuming the nature of its unseen trees. But new technologies have generated masses of genomic data that raise unexpected challenges to a prevailing view that grew from a theory that melded Darwinian selection and Mendelian genetic causation. Both rested on direct, largely deterministic, and highly simplified concepts of the relationship between genes and what they do. Darwin believed that natural selection was a fine-tuning mechanism that screened competing individuals to detect even the smallest difference among them. The causal elements weren’t known, but one could assume their existence, as Darwin did, and study the organisms they produced. If selection were universal, then biological functions must have adaptive explanations. Meanwhile, the inheritance that Mendel documented was probabilistic, but in a very limited and rigid way, with fixed probabilities and a few genetically determined outcome states. The discovery of Mendelian determinism led to an extremely effective genetic research program that discovered the nature, location, and arrangement of genes and their protein-coding function, whose legacy we are reaping today. Although Darwin’s and Mendel’s work developed independently and seemed to be addressing separate questions, by the 1930s these had been connected into a single, simple genetic understanding of life. However, the new data are revealing how complex life’s genetic underpinnings actually are. Within each cell, more than six billion nucleotides of DNA encode countless thousands of functional elements. Each of our hundreds of types of cells uses these elements differently, in different contexts; each element can vary among individuals and even among cells, because mutations occur in them during life. The challenge to understand this complexity is daunting, and some rethinking is in order. The data are revealing deep but subtle unity of genetic and evolutionary causation. Some of these similarities are summarized in Figure 1. For example, most alleles (variants at a given position in the genome) have low frequency in the population, a relatively local geographic distribution, and small effects on phenotypes, while common, geographically widespread, large-effect alleles are rarer. If we digest this new knowledge, findings that have been seen as mysterious are easily explained. But sometimes what we can detect contributes less, and what we can’t detect contributes more to our understanding of life than has generally been thought.

Climate-driven population divergence in sex-determining systems

Sex determination is a fundamental biological process, yet its mechanisms are remarkably diverse. In vertebrates, sex can be determined by inherited genetic factors or by the temperature experienced during embryonic development. However, the evolutionary causes of this diversity remain unknown. Here we show that live-bearing lizards at different climatic extremes of the species' distribution differ in their sex-determining mechanisms, with temperature-dependent sex determination in lowlands and genotypic sex determination in highlands. A theoretical model parameterized with field data accurately predicts this divergence in sex-determining systems and the consequence thereof for variation in cohort sex ratios among years. Furthermore, we show that divergent natural selection on sex determination across altitudes is caused by climatic effects on lizard life history and variation in the magnitude of between-year temperature fluctuations. Our results establish an adaptive explanation for intra-specific divergence in sex-determining systems driven by phenotypic plasticity and ecological selection, thereby providing a unifying framework for integrating the developmental, ecological and evolutionary basis for variation in vertebrate sex determination.

Beyond splitting hares and rabbiting on about major histocompatibility complex complexity.

The genes of the major histocompatibility complex (MHC) have become the target of choice for studies wishing to examine adaptively important genetic diversity in natural populations. Within Molecular Ecology alone, there have been 71 papers on aspects of MHC evolution over the past few years, with an increasing year on year trend. This focus on the MHC is partly driven by the hypothesized links between MHC gene dynamics and ecologically interesting and relevant traits, such as mate choice and host–parasite interactions. However, an ability to pin down the evolutionary causes and ecological consequences of MHC variation in natural populations has proven challenging and has been hampered by the very issue that is attractive about MHC genes – their high levels of diversity. Linking high levels of MHC diversity to ecological factors in inherently complex natural populations requires a level of experimental design and analytical rigour that is extremely difficult to achieve owing to a plethora of potentially confounding and interacting variables. In this issue of Molecular Ecology, Smith et al. (2010) elegantly overcome the challenge of detecting complex interactions in complex systems by using an intricate analytical approach to demonstrate a role for MHC in the reproductive ability of a natural population of the European hare Lepus europaeus (Fig. 1). Also in this issue, Oppelt et al. (2010) demonstrate a role for MHC variation in determining levels of hepatic coccidian infection in the European rabbit Oryctolagus cuniculus (Fig. 2).

Evolutionary causes and consequences of consistent individual variation in cooperative behaviour.

Behaviour is typically regarded as among the most flexible of animal phenotypic traits. In particular, expression of cooperative behaviour is often assumed to be conditional upon the behaviours of others. This flexibility is a key component of many hypothesized mechanisms favouring the evolution of cooperative behaviour. However, evidence shows that cooperative behaviours are often less flexible than expected and that, in many species, individuals show consistent differences in the amount and type of cooperative and non-cooperative behaviours displayed. This phenomenon is known as 'animal personality' or a 'behavioural syndrome'. Animal personality is evolutionarily relevant, as it typically shows heritable variation and can entail fitness consequences, and hence, is subject to evolutionary change. Here, we review the empirical evidence for individual variation in cooperative behaviour across taxa, we examine the evolutionary processes that have been invoked to explain the existence of individual variation in cooperative behaviour and we discuss the consequences of consistent individual differences on the evolutionary stability of cooperation. We highlight that consistent individual variation in cooperativeness can both stabilize or disrupt cooperation in populations. We conclude that recognizing the existence of consistent individual differences in cooperativeness is essential for an understanding of the evolution and prevalence of cooperation.

Comprehensive paternity assignment: genotype, spatial location and social status in song sparrows, Melospiza Melodia

Comprehensive, accurate paternity assignment is critical to answering numerous questions in evolutionary ecology. Yet, most studies of species with extra-pair paternity (EPP) fail to assign sires to all offspring. Common limitations include incomplete and biased sampling of offspring and males, particularly with respect to male location and social status, potentially biasing estimated patterns of paternity. Studies that achieve comprehensive sampling and paternity assignment are therefore required. Accordingly, we genotyped virtually all males and >99% of 6-day-old offspring over 16 years in a song sparrow (Melospiza melodia) population and used three complementary statistical methodologies to attempt complete paternity assignment for all 2207 offspring. Assignments were highly consistent across maximum likelihood methods that used solely genotype data, and heuristic and integrated Bayesian analyses that included data describing individual locations. Sires were assigned to >99% of all genotyped offspring with ≥95% confidence, revealing an EPP rate of c. 28%. Extra-pair sires primarily occupied territories neighbouring their extra-pair offspring; spatial location was therefore highly informative for paternity assignment. EPP was biased towards paired territorial males, although unpaired territorial and floater males sired c. 13% of extra-pair offspring. Failing to sample and include unpaired males as candidate sires would therefore substantially reduce assignment rates. These analyses demonstrate the integration of genetic and ecological information to achieve comprehensive paternity assignment and direct biological insight, illustrate the potential biases that common forms of incomplete sampling could have on estimated patterns of EPP, and provide an essential basis for understanding the evolutionary causes and consequences of EPP.

Genetics and the causes of evolution: 150 years of progress since Darwin

The publication of The Origin of Species in 1859 represents an unsurpassed landmark in the history of biology. Charles Darwin had been thinking about evolution since 1836, and accumulating evidence both that it had occurred and that it was caused primarily (but not exclusively, as he was always

The role of threats in animal cooperation.

In human societies, social behaviour is strongly influenced by threats of punishment, even though the threats themselves rarely need to be exercised. Recent experimental evidence suggests that similar hidden threats can promote cooperation and limit within-group selfishness in some animal systems. In other animals, however, threats appear to be ineffective. Here I review theoretical and empirical studies that help to understand the evolutionary causes of these contrasting patterns, and identify three factors—impact, accuracy and perception—that together determine the effectiveness of threats to induce cooperation.