The behavioural ecology of personality: consistent individual differences from an adaptive perspective

Individual humans, and members of diverse other species, show consistent differences in aggressiveness, shyness, sociability and activity. Such intraspecific differences in behaviour have been widely assumed to be non‐adaptive variation surrounding (possibly) adaptive population‐average behaviour. Nevertheless, in keeping with recent calls to apply Darwinian reasoning to ever‐finer scales of biological variation, we sketch the fundamentals of an adaptive theory of consistent individual differences in behaviour. Our thesis is based on the notion that such ‘personality differences’ can be selected for if fitness payoffs are dependent on both the frequencies with which competing strategies are played and an individual's behavioural history. To this end, we review existing models that illustrate this and propose a game theoretic approach to analyzing personality differences that is both dynamic and state‐dependent. Our motivation is to provide insights into the evolution and maintenance of an apparently common animal trait: personality, which has far reaching ecological and evolutionary implications.     

Flexibility in reproductive timing in human females: integrating ultimate and proximate explanations

From an ultimate perspective, the age of onset of female reproduction should be sensitive to variation in mortality rates, and variation in the productivity of non-reproductive activities. In accordance with this prediction, most of the cross-national variation in women's age at first birth can be explained by differences in female life expectancies and incomes. The within-country variation in England shows a similar pattern: women have children younger in neighbourhoods where the expectation of healthy life is shorter and incomes are lower. I consider the proximate mechanisms likely to be involved in producing locally appropriate reproductive decisions. There is evidence suggesting that developmental induction, social learning and contextual evocation may all play a role.     

The effects of ecology on life history strategies and metabolic disturbances during development: an example from the African bovids

Life history theory predicts environmental factors to affect changes in life history strategies. However, owing to the interrelationships between body mass and life history variables, it is difficult to discern causal relationships, especially in large-bodied mammals and using a comparative approach. The situation is exacerbated in palaeobiologi-cal studies, where many of the variables cannot be observed directly. Specifically, mortality risk has been identified as one of the most important factors determining life history strategies, but its assessment is difficult. This hampers analyses of life history evolution. This study thus explored the possibility to extract previously untapped information from hard tissue, i.e. teeth, which may be useful for life history reconstruction. Histological sections of 25 molars of bovids, representing all subfamilies and spanning a wide range of body masses, were analysed with regard to: (i) molar crown formation times in relation to female body mass and gestation length, and (ii) metabolic disturbances from early to late forming teeth in relation to habitat type occupied, diet consumed and habitual walking style employed. It was found that molar crown formation times in bovids are highly correlated with gestation length once the effects of body mass have been removed. This differs from primates and indicates similarities in pre- and postnatal growth rates in these mammals. Closed-habitat species exhibit relatively fewer disturbances during development than open-country species, but the reverse holds for adult specimens. This accords with what is known about the ecological and behavioural adaptations of the species and is predicted by life history theory. It could thus be confirmed that teeth may provide vital information about life history variables. Exploitation of this information will allow hypotheses to be tested regarding the evolutionary changes in life history strategies of extinct species.     

Molecular adaptation of ammonia monooxygenase during independent pH specialization in Thaumarchaeota

Microbes are abundant in nature and often highly adapted to local conditions. While great progress has been made in understanding the ecological factors driving their distribution in complex environments, the underpinning molecular‐evolutionary mechanisms are rarely dissected. Therefore, we scrutinized the coupling of environmental and molecular adaptation in Thaumarchaeota, an abundant archaeal phylum with a key role in ammonia oxidation. These microbes are adapted to a diverse spectrum of environmental conditions, with pH being a key factor shaping their contemporary distribution and evolutionary diversification. We integrated high‐throughput sequencing data spanning a broad representation of ammonia‐oxidizing terrestrial lineages with codon modelling analyses, testing the hypothesis that ammonia monooxygenase subunit A (AmoA) – a highly conserved membrane protein crucial for ammonia oxidation and classical marker in microbial ecology – underwent adaptation during specialization to extreme pH environments. While purifying selection has been an important factor limiting AmoA evolution, we identified episodic shifts in selective pressure at the base of two phylogenetically distant lineages that independently adapted to acidic conditions and subsequently gained lasting ecological success. This involved nonconvergent selective mechanisms (positive selection vs. selection acting on variants fixed during an episode of relaxed selection) leading to unique sets of amino acid substitutions that remained fixed across the radiation of both acidophilic lineages, highlighting persistent adaptive value in acidic environments. Our data demonstrates distinct trajectories of AmoA evolution despite convergent phenotypic adaptation, suggesting that microbial environmental specialization can be associated with diverse signals of molecular adaptation, even for marker genes employed routinely by microbial ecologists.     

Temperature and embryonic development in polar marine invertebrates

The life-history tactics of many Antarctic marine invertebrates suggest that the commonly observed slow rates of growth are adaptations to the pattern of food availability, and not due to low temperature per se. This implies that marine invertebrates have been able, over the course of evolutionary time, to compensate their rates of embryonic development for the effect of temperature. Data from north Atlantic copepods indicate that this is so. It is therefore suggested that the slow rates of embryonic development in many Antarctic marine invertebrates are the result of large egg size, and not the low temperature. Large, slowly developing eggs are part of a suite of tactics, often called K-strategies, which characterise many marine invertebrates in Antarctica.     

Evolution and plasticity of anuran larval development in response to desiccation. A comparative analysis

Anurans breed in a variety of aquatic habitats with contrasting levels of desiccation risk, which may result in selection for faster development during larval stages. Previous studies suggest that species in ephemeral ponds reduce their developmental times to minimize desiccation risks, although it is not clear how variation in desiccation risk affects developmental strategies in different species. Employing a comparative phylogenetic approach including data from published and unpublished studies encompassing 62 observations across 30 species, we tested if species breeding in ephemeral ponds (High risk) develop faster than those from permanent ponds (Low risk) and/or show increased developmental plasticity in response to drying conditions. Our analyses support shorter developmental times in High risk, primarily by decreasing body mass at metamorphosis. Plasticity in developmental times was small and did not differ between groups. However, accelerated development in High risk species generally resulted in reduced sizes at metamorphosis, while some Low risk species were able compensate this effect by increasing mean growth rates. Taken together, our results suggest that plastic responses in species breeding in ephemeral ponds are constrained by a general trade-off between development and growth rates.     

Parallel invasions produce heterogenous patterns of life history adaptation: rapid divergence in an invasive insect

Biotic invasions provide a natural experiment in evolution: when invasive species colonize new ranges, they may evolve new clines in traits in response to environmental gradients. Yet it is not clear how rapidly such patterns can evolve and whether they are consistent between regions. We compare four populations of the invasive cabbage white butterfly (Pieris rapae) from North America and Japan, independently colonized by P. rapae 150 years ago and 300 years ago, respectively. On each continent, we employed a northern and southern population to compare the effects of latitude on body mass, development rate and immune function. For each population, we used a split‐sibling family design in which siblings were reared at either warm (26.7 °C) or cool (20 °C) temperatures to determine reaction norms for each trait. Latitudinal patterns in development time were similar between the two continents. In contrast, there were strong geographical differences in reaction norms for body size, but no consistent effects of latitude; there were no detectable effects of latitude or continent on immune function. These results imply that some life history traits respond consistently to selection along climatic gradients, whereas other traits may respond to local environmental factors, or not at all.     

进化生态学的产生与发展

进化论、遗传学与生态学是在不同时期发展起来的独立学科,然而,随着科学的发展,们越来越认识到它们之间存在着密切的关系。Petrusewicz(1959)(见Shvarts,1977)曾写过《达尔文进化论是一种生态理论》一书,强调进化在本质上是一生态过程。Hutchinson(1965)写了一部题名为《生态学舞台和进化节目》一书,认为生态的布景可以作为进化过程的舞台。但是,最早提出进化生态学这一概念的则是Orians(1962)。进化生态学从产生到现在虽然只有20多年的历史,但已成为生态学研究的重要领域。下面从几个方面谈谈进化生态学的产生与发展。     

Evolution of a plastic quantitative trait in an age-structured population in a fluctuating environment

We analyze weak fluctuating selection on a quantitative character in an age-structured population not subject to density regulation. We assume that early in the first year of life before selection, during a critical state of development, environments exert a plastic effect on the phenotype, which remains constant throughout the life of an individual. Age-specific selection on the character affects survival and fecundity, which have intermediate optima subject to temporal environmental fluctuations with directional selection in some age classes as special cases. Weighting individuals by their reproductive value, as suggested by Fisher, we show that the expected response per year in the weighted mean character has the same form as for models with no age structure. Environmental stochasticity generates stochastic fluctuations in the weighted mean character following a first-order autoregressive model with a temporally autocorrelated noise term and stationary variance depending on the amount of phenotypic plasticity. The parameters of the process are simple weighted averages of parameters used to describe age-specific survival and fecundity. The "age-specific selective weights" are related to the stable distribution of reproductive values among age classes. This allows partitioning of the change in the weighted mean character into age-specific components.     

Developmental strategies in an invasive spider: constraints and plasticity

1. Growth defines the major life‐history traits such as size, weight, and age at maturity that determine an organism's fitness. Different models have been developed to describe growth by means of geometric progressions (e.g. Dyar's rule). However, growth forced along a geometric trajectory might constrain a plastic response to variable environmental conditions (e.g. food availability). 2. The present study investigated growth patterns under varying food conditions in the bridge spider, Larinioides sclopetarius, an extremely successful species in colonising urban habitats. 3. In L. sclopetarius growth ratios of successive instars were not constant but decreased over development. Instead, these spiders' growth is well described by a developmental growth rate (weight gain per moult) and a growth coefficient (weight gain per development time), both of which are based on a geometric progression. All developmental parameters, including developmental growth rate and growth coefficient as well as the intermoult duration and the number of instars, highly depend on food availability in L. sclopetarius and thus show plasticity. 4. Our study shows that geometric growth patterns do not necessarily preclude plasticity and that the parameters of geometric growth are affected by developmental plasticity. We suggest that their high developmental plasticity may facilitate bridge spiders' success in invading urban habitats.     

Evolution of chinook salmon (Oncorhynchus tshawytscha) populations in New Zealand: pattern,rate, and process

Chinook salmon, Oncorhynchus tshawytscha, from the Sacramento River, California, USA were introduced to New Zealand between 1901 and 1907, and colonized most of their present-day range within about 10 years. The New Zealand populations now vary in phenotypic traits typically used to differentiate salmon populations within their natural range: growth in freshwater and at sea, age at maturity, dates of return to fresh water and reproduction, morphology, and reproductive allocation. This paper reviews a large research program designed to determine the relative contributions of phenotypic plasticity and genetic adaptation to this variation, in an effort to understand the processes underlying the natural evolution of new populations. We found strong evidence of trait divergence between populations within at most 30 generations, particularly in freshwater growth rate, date of return, and reproductive output, with plausible adaptive bases for these differences. Importantly, we also demonstrated not only a genetic basis for post-release survival but higher survival, and hence fitness, of a population released from its established site compared to another population released from the same site. We conclude that divergence of salmon in different rivers probably resulted initially from phenotypic plasticity (e.g., habitat-specific growth rates, and effects of upriver migration on ovarian investment). Philopatry (homing to natal streams) combined with rapid evolution of distinct breeding periods to restrict gene flow, facilitating divergence in other traits. We also suggest that in addition to genetic divergence resulting from random founder effects, divergence may also arise during the very early stages of colonization when the original colonists are a non-random, pre-adapted subset of the source population. This favored founders effect immediately improves the fitness of the new population. Overall, this research reveals the complex interplay of environmental and genetic controls over behavior, physiology and life history that characterize the early stages of population differentiation, a process that has taken place repeatedly during the history of salmon populations.     

Context-dependent sexual advertisement: plasticity in development of sexual ornamentation throughout the lifetime of a passerine bird

Male investment into sexual ornamentation is a reproductive decision that depends on the context of breeding and life history state. In turn, selection for state- and context-specific expression of sexual ornamentation should favour the evolution of developmental pathways that enable the flexible allocation of resources into sexual ornamentation. We studied lifelong variation in the expression and condition-dependence of a sexual ornament in relation to age and the context of breeding in male house finches (Carpodacus mexicanus)--a species that develops a new sexual ornament once a year after breeding. Throughout males' lifetime, the elaboration of ornamentation and the allocation of resources to the development of sexual ornamentation depended strongly on pairing status in the preceding breeding season--males that were single invested more resources into sexual ornamentation and changed ornamentation more than males that were paired. During the initial (post-juvenile) moult, the expression of ornamentation was closely dependent on individual condition, however the condition-dependence of ornamentation sharply decreased throughout a male's lifetime and in older males expression of sexual ornamentation was largely independent of condition during moult. Selection for early breeding favoured greater ornamentation in males that were single in the preceding seasons and the strength of this selection increased with age. On the contrary, the strength of selection on sexual ornamentation decreased with age in males that were paired in the preceding breeding season. Our results reveal strong context-dependency in investment into sexual ornamentation as well as a high flexibility in the development of sexual ornamentation throughout a male's life.     

Flowering time QTL in natural populations of Arabidopsis thaliana and implications for their adaptive value

The genetic basis of phenotypic traits is of great interest to evolutionary biologists, but their contribution to adaptation in nature is often unknown. To determine the genetic architecture of flowering time in ecologically relevant conditions, we used a recombinant inbred line population created from two locally adapted populations of Arabidopsis thaliana from Sweden and Italy. Using these RILs, we identified flowering time QTL in growth chambers that mimicked the natural temperature and photoperiod variation across the growing season in each native environment. We also compared the genomic locations of flowering time QTL to those of fitness (total fruit number) QTL from a previous three‐year field study. Ten total flowering time QTL were found, and in all cases, the Italy genotype caused early flowering regardless of the conditions. Two QTL were consistent across chamber environments, and these had the largest effects on flowering time. Five of the fitness QTL colocalized with flowering time QTL found in the Italy conditions, and in each case, the local genotype was favoured. In contrast, just two flowering time QTL found in the Sweden conditions colocalized with fitness QTL and in only one case was the local genotype favoured. This implies that flowering time may be more important for adaptation in Italy than Sweden. Two candidate genes (FLC and VIN3) underlying the major flowering time QTL found in the current study are implicated in local adaptation.     

Reverse evolution of fitness in Drosophila melanogaster

Abstract The evolution of fitness is central to evolutionary theory, yet few experimental systems allow us to track its evolution in genetically and environmentally relevant contexts. Reverse evolution experiments allow the study of the evolutionary return to ancestral phenotypic states, including fitness. This in turn permits well‐defined tests for the dependence of adaptation on evolutionary history and environmental conditions. In the experiments described here, 20 populations of heterogeneous evolutionary histories were returned to their common ancestral environment for 50 generations, and were then compared with both their immediate differentiated ancestors and populations which had remained in the ancestral environment. One measure of fitness returned to ancestral levels to a greater extent than other characters did. The phenotypic effects of reverse evolution were also contingent on previous selective history. Moreover, convergence to the ancestral state was highly sensitive to environmental conditions. The phenotypic plasticity of fecundity, a character directly selected for, evolved during the experimental time frame. Reverse evolution appears to force multiple, diverged populations to converge on a common fitness state through different life‐history and genetic changes.     

Ecology of Naididae (Oligochaeta) from an alkaline bog stream: life history patterns and community structure

Population and community dynamics of naidid oligochaetes were studied from June 1982–December 1983 in a sluggish, alkaline bog stream situated within Cedarburg Bog, Ozaukee County, Wisconsin, USA. Temporal differences in periods of peak abundance were observed for five species studied in detail: Chaetogaster diaphanus (mid-August and September), Chaetogaster diastrophus (mid-May), Dero digitata (mid-September), Dero nivea (mid-October), and Pristina leidyi (mid-October). Several correlations of abiotic and biotic parameters to density and percentage of naidids reproducing asexually were calculated. Mean doubling times (days) for field populations were 12.1, 22.7, 62.4, 19.6, 27.7 for C. diaphanus, C. diastrophus, D. digitata, D. nivea, and P. leidyi, respectively. Asexual reproduction by paratomy was the principal method of population increase. Sexual specimens were observed for Stylaria lacustris during June and October–December, D. digitata in September, C. diastrophus and Nais simplex during October, and C. diaphanus in October–November. Generally, a high proportion of the respective population was sexually mature when this type of reproduction occurred. Naididae community diversity index values using the Shannon-Weaver index ranged from 0.19–3.86.     

Adaptive contraction of diet breadth affects sexual maturation and specific nutrient consumption in an extreme generalist omnivore

Animals balance their intake of specific nutrients, but little is known about how they do so when foraging in an environment with toxic resources and whether toxic foods promote adaptations that affect life history traits. In German cockroach (Blattella germanica) populations, glucose aversion has evolved in response to glucose‐containing insecticidal baits. We restricted newly eclosed glucose‐averse (GA) and wild‐type (WT) female cockroaches to nutritionally defined diets varying in protein‐to‐carbohydrate (P : C) ratio (3 : 1, 1 : 1, or 1 : 3) or gave them free choice of the 3 : 1 and 1 : 3 diets, with either glucose or fructose as the sole carbohydrate source. We measured consumption of each diet over 6 days and then dissected the females to measure the length of basal oocytes in their ovaries. Our results showed significantly lower consumption by GA compared to WT cockroaches when restricted to glucose‐containing diets, but also lower fructose intake by GA compared to WT cockroaches when restricted to high fructose diets or given choice of fructose‐containing diets. Protein intake was regulated tightly regardless of carbohydrate intake, except by GA cockroaches restricted to glucose‐containing diets. Oocyte growth was completely suppressed in GA females restricted to glucose‐containing diets, but also significantly slower in GA than in WT females restricted to fructose‐containing diets. Our findings suggest that GA cockroaches have adapted to reduced diet breadth through endocrine adjustments which reduce requirements for energetic fuels. Our study illustrates how an evolutionary change in the chemosensory system may affect the evolution of other traits that govern animal life histories.     

Dynamic changes in DNA methylation during embryonic and postnatal development of an altricial wild bird

DNA methylation could shape phenotypic responses to environmental cues and underlie developmental plasticity. Environmentally induced changes in DNA methylation during development can give rise to stable phenotypic traits and thus affect fitness. In the laboratory, it has been shown that the vertebrate methylome undergoes dynamic reprogramming during development, creating a critical window for environmentally induced epigenetic modifications. Studies of DNA methylation in the wild are lacking, yet are essential for understanding how genes and the environment interact to affect phenotypic development and ultimately fitness. Furthermore, our knowledge of the establishment of methylation patterns during development in birds is limited. We quantified genome‐wide DNA methylation at various stages of embryonic and postnatal development in an altricial passerine bird, the great tit Parus major. While, there was no change in global DNA methylation in embryonic tissue during the second half of embryonic development, a twofold increase in DNA methylation in blood occurred between 6 and 15 days posthatch. Though not directly comparable, DNA methylation levels were higher in the blood of nestlings compared with embryonic tissue at any stage of prenatal development. This provides the first evidence that DNA methylation undergoes global change during development in a wild bird, supporting the hypothesis that methylation mediates phenotypic development. Furthermore, the plasticity of DNA methylation demonstrated during late postnatal development, in the present study, suggests a wide window during which DNA methylation could be sensitive to environmental influences. This is particularly important for our understanding of the mechanisms by which early‐life conditions influence later‐life performance. While, we found no evidence for differences in genome‐wide methylation in relation to habitat of origin, environmental variation is likely to be an important driver of variation in methylation at specific loci.     

Primate milk: proximate mechanisms and ultimate perspectives

To understand the evolutionary forces that have shaped primate lactation strategies, it is important to understand the proximate mechanisms of milk synthesis and their ecological and phylogenetic contexts. The lactation strategy of a species has four interrelated dimensions: the frequency and duration of nursing bouts, the period of lactation until weaning, the number and sex ratio of infants that a mother rears simultaneously, and the composition and yield of the milk that mothers synthesize. Milk synthesis, arguably the most physiologically costly component of rearing infants, remains the least studied. Energy transfer becomes energetically less efficient, transitioning from placental support to milk synthesis just as the energy requirements for infant growth, development, and behavioral activity substantially increase. Here we review primate lactation biology and milk synthesis, integrating studies from anthropology, biology, nutrition, animal science, immunology, and biochemistry, to identify the derived and ancestral features of primate milks and enhance our understanding of primate life history.