Jon E. Brommer

On between-individual and residual (co)variances in the study of animal personality: are you willing to take the “individual gambit”?

SummaryA recent discussion in this journal (Dingemanse et al. Behav Ecol Sociobiol 66: 1543–1548, 2012; Garamszegi and Herczeg Behav Ecol Socibiol 66:1651–1658, 2012) deals with a core issue in animal personality research: Can animal personality research quantify correlated behaviors on the between-individual level, or is this too demanding in terms of design and analysis of the data, and should behavioral ecologists therefore take the “individual gambit” and work on the phenotypic level only. Taking this gambit implies accepting that the between-individual correlation in behavioral traits (which is the correlation of interest) may be masked by a residual correlation of different magnitude or sign. Understanding (co)variances on different levels is the main thrust of quantitative genetics, and animal personality research can make good use of the plethora of ideas and analytical approaches developed in this field. I, here, outline reasons why the “individual gambit” may or may not work out and its relationship to the quantitative genetic “phenotypic gambit”. I especially emphasize the meaning of residuals and phenotypic plasticity which has not been fully appreciated in the debate thus far. I conclude that instead of a priori assuming that between-individual correlations are captured sufficiently well by the phenotypic correlation, animal personality researchers should set up more ambitious data collection and analysis designs to critically test this conjectured equality.

Exploring the genetics of nestling personality traits in a wild passerine bird: testing the phenotypic gambit.

When several personality traits covary, they form a behavioral syndrome. Understanding the evolutionary dynamics of a behavioral syndrome requires knowledge of its genetic underpinning. At present, our understanding of the genetic basis of behavioral syndromes is largely restricted to domestic and laboratory animals. Wild behavioral syndromes are mostly inferred on the basis of phenotypic correlations, and thus make the “phenotypic gambit” of assuming that these phenotypic correlations capture the underlying genetic correlations. On the basis of 3 years of reciprocal cross-fostering of 2896 nestlings of 271 families within a pedigreed population, we show that the nestling personality traits handling aggression, breathing rate, and docility are heritable (h2 = 16–29%), and often have a pronounced “nest-of-rearing” variance component (10–15%), but a relatively small “nest-of-origin” variance component (0–7%). The three nestling personality traits form a behavioral syndrome on the phenotypic and genetic level. Overall, the phenotypic correlations provide a satisfactory description of the genetic ones, but significantly underestimate the magnitude of one of the pairwise genetic correlations, which mirrors the conclusion based on domestic and laboratory studies.

Testing for between individual correlations of personality and physiological traits in a wild bird

Recently, integration of personality traits into a ‘pace-of-life syndrome’ (POLS) context has been advocated. To be able to understand how an individual’s behavioural, physiological and life history traits may coevolve, we need to jointly quantify these traits in order to study their covariance. Few studies have established links between personality and immunity properties of an individual. We here examined covariation of a measure of skeletal size (tarsus length), three behavioural traits (activity, handling aggression and breath rate) and two immunological traits (IgG level and haematocrit), in 592 wild caught blue tits. Many individuals (201) were tested more than once, allowing quantification of individual consistency of all traits and partition of the covariances between the traits, using a multivariate mixed model, into between individual and residual covariances. We find individual consistency of all behavioural traits, indicating that these capture aspects of blue tit adult personality and also the physiological measures are repeatable. Contrary to the POLS expectation, we find no overall significant individual level correlation structure between these traits and a factor analytical approach confirmed that between individual correlations across traits were not due to a common (POLS) factor or driven by size (tarsus length). Based on a published power study, we conclude that there is no common syndrome of individual level covariance between personality and physiological traits in wild blue tits or that the effect sizes, such a syndrome generates, are too low (r < 0.3) to detect. Future field-based work should be designed to explore low effect sizes and strive to measure specific traits whose involvement is implicated to have large effect sizes as based on, e.g. laboratory findings.

Range margin shifts of birds revisited – the role of spatiotemporally varying survey effort

Global climate warming is predicted to lead to global and regional changes in the distribution of organisms. One influential approach to test this prediction using temporally repeated mapping surveys of organisms was suggested in a seminal paper by Thomas & Lennon (1999, Nature). The Thomas & Lennon approach corrects observed changes in the range margin for changes in the range size, and thus potentially controls for other broad-scale environmental changes between surveys, however the approach does not necessarily account for potential biases in sampling effort. To verify whether the issue of variation in sampling effort affects empirical estimates of shifts in range margin, we reanalyzed all three published studies exploring range margin changes of breeding birds in Great Britain (GB), Finland, and New York State (NY). Accounting for changes in survey effort on range margins lowered the estimated shift for breeding birds in New York, but the shift remained statistically significant. For Great Britain and Finland, for which no direct estimate of survey effort is available, we used species richness (a strong correlate of survey effort in New York) as a proxy and found that in both cases the estimated shift in range margin was significantly reduced and became nonsignificant. To understand how robust the approach is to sampling biases, we use a simulation model to show that the Thomas & Lennon approach is, under certain conditions, sensitive to changes in detection probability (probability to detect true occupancy) which in turn may be affected by changes in surveying effort between surveys. We thus found evidence that temporal changes in the distribution of breeding birds based on repeated mapping surveys may be inflated by changes in survey effort along range boundaries. We discuss possible approaches to deal with this issue in the analysis and design of national or regional surveys.

Variation in plasticity of personality traits implies that the ranking of personality measures changes between environmental contexts: calculating the cross-environmental correlation

Studies increasingly explore whether there is variation between individuals in how they adjust their behavior to different environmental contexts using random regression analysis (RR). RR estimates the between-individual variance in elevation (expected behavior in the mean environment) and variance in plasticity (individual-specific adjustment of behavior to the environment) and the covariance between these properties. These (co)variances allow deriving both environment-specific repeatability estimates and the individual-level correlation in behavior between environmental conditions, both of which are of key interest for understanding consistency in behavior over space and time, a core issue in animal personality research. However, very few studies use the RR estimates to produce this information. In this paper, I outline how to extract this information (including example code in R) and apply the approach to 16 estimates based on nine published RR studies. Despite the fact that the behaviors have a decent repeatability under different environmental conditions, I find that in half the cases, the cross-environmental correlation is low (<0.4). This implies that individuals differ in their behavioral trait values but that the ranking of these individual values tends to change between environmental conditions. This level of inconsistency in animal personality traits appears not to have been fully appreciated, and future studies on plasticity using RR should explicitly include it.

Demographic routes to variability and regulation in bird populations

There is large interspecific variation in the magnitude of population fluctuations, even among closely related species. The factors generating this variation are not well understood, primarily because of the challenges of separating the relative impact of variation in population size from fluctuations in the environment. Here, we show using demographic data from 13 bird populations that magnitudes of fluctuations in population size are mainly driven by stochastic fluctuations in the environment. Regulation towards an equilibrium population size occurs through density-dependent mortality. At small population sizes, population dynamics are primarily driven by environment-driven variation in recruitment, whereas close to the carrying capacity K, variation in population growth is more strongly influenced by density-dependent mortality of both juveniles and adults. Our results provide evidence for the hypothesis proposed by Lack that population fluctuations in birds arise from temporal variation in the difference between density-independent recruitment and density-dependent mortality during the non-breeding season.

A strong genetic correlation underlying a behavioural syndrome disappears during development because of genotype–age interactions

In animal populations, as in humans, behavioural differences between individuals that are consistent over time and across contexts are considered to reflect personality, and suites of correlated behaviours expressed by individuals are known as behavioural syndromes. Lifelong stability of behavioural syndromes is often assumed, either implicitly or explicitly. Here, we use a quantitative genetic approach to study the developmental stability of a behavioural syndrome in a wild population of blue tits. We find that a behavioural syndrome formed by a strong genetic correlation of two personality traits in nestlings disappears in adults, and we demonstrate that genotype–age interaction is the likely mechanism underlying this change during development. A behavioural syndrome may hence change during organismal development, even when personality traits seem to be strongly physiologically or functionally linked in one age group. We outline how such developmental plasticity has important ramifications for understanding the mechanistic basis as well as the evolutionary consequences of behavioural syndromes.

INTERACTIONS BETWEEN GENOTYPE AND SEXUAL CONFLICT ENVIRONMENT INFLUENCE TRANSGENERATIONAL FITNESS IN DROSOPHILA MELANOGASTER

Theory predicts that sexual conflict can fuel evolutionary change and generate substantial reproductive costs. This was tested here by measuring the fitness of focal individuals across multiple generations using an experimental framework. We manipulated sexual conflict through high versus low exposure of females to males across a four‐generation pedigree of Drosophila melanogaster, and assessed fitness in 1062 females and 639 males. We used the animal model to estimate (1) genotype by sexual conflict environment interactions for female fitness and (2) indirect benefits gained through sons and daughters. Some female genotypes achieved higher fitness under low, in comparison to high, conflict and vice versa. We found a consistent 10% reduction in female fitness under high conflict, regardless of maternal history. Following high exposure, females produced sons with increased, but grandsons with decreased, fitness. This opposing effect suggests no consistent fitness gains through sons for females that mated multiply. We saw no indirect benefits through daughters. Our pedigree was based exclusively on maternal links; however, maternal effects are unlikely to contribute significantly unless expressed across multiple generations. In sum, we quantified a significant sexual conflict load and a female genotype by sexual conflict interaction that could slow the erosion of genetic variation.

The importance of genotype-by-age interactions for the development of repeatable behavior and correlated behaviors over lifetime.

Behaviors are highly plastic and one aspect of this plasticity is behavioral changes over age. The presence of age-related plasticity in behavior opens up the possibility of between-individual variation in age-related plasticity (Individual-Age interaction, IxA) and genotype-age interaction (GxA). We outline the available approaches for quantifying GxA. We underline that knowledge of GxA for behaviors is an important step in reaching and understanding of the evolution of plasticity in behavior over lifetime. In particular, the heritability (repeatability) and/or the rank order of behavior across individuals are predicted to change across ages in presence of GxA. We draw on the theory of reaction norms to illustrate that GxA, when present, is likely to lead to developmental changes in the magnitude and possibly sign of the genetic correlation between behaviors (behavioral syndrome). We present an overview of the literature on changes in the ranking of individuals’ behavior across ages, and in the correlation between behaviors. Although all studies were carried out on the phenotypic level, they overall suggest clear scope for increased study of GxA as a process explaining age-related plasticity in behaviors. Lastly, we throughout emphasize that many of the approaches and underlying theory of GxA is applicable to the study of IxA, which is informative as it presents the upper limit of GxA, but is also a more attainable target of study in many systems. Empirical work aimed at understanding IxA and GxA in behavior is needed in order to understand whether patterns predicted by theory on plasticity indeed occur for age-related plasticity of behavior.

Size differentiation in Finnish house sparrows follows Bergmann's rule with evidence of local adaptation

Bergmanns rule predicts that individuals are larger in more poleward populations and that this size gradient has an adaptive basis. Hence, phenotypic divergence in size traits between populations (PST) is expected to exceed the level of divergence by drift alone (FST). We measured 16 skeletal traits, body mass and wing length in 409 male and 296 female house sparrows Passer domesticus sampled in 12 populations throughout Finland, where the species has its northernmost European distributional margin. Morphometric differentiation across populations (PST) was compared with differentiation in 13 microsatellites (FST). We find that twelve traits phenotypically diverged more than FST in both sexes, and an additional two traits diverged in males. The phenotypic divergence exceeded FST in several traits to such a degree that findings were robust also to strong between‐population environmental effects. Divergence was particularly strong in dimensions of the bill, making it a strong candidate for the study of adaptive molecular genetic divergence. Divergent traits increased in size in more northern populations. We conclude that house sparrows show evidence of an adaptive latitudinal size gradient consistent with Bergmanns rule on the modest spatial scale of ca. 600 km.