Martijn van de Pol

A simple method for distinguishing within- versus between-subject effects using mixed models

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MHC-dependent survival in a wild population: evidence for hidden genetic benefits gained through extra-pair fertilizations.

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Strategic promiscuity helps avoid inbreeding at multiple levels in a cooperative breeder where both sexes are philopatric

Females should prefer to be fertilized by males that increase the genetic quality of their offspring. In vertebrates, genes of the major histocompatibility complex (MHC) play a key role in the acquired immune response and have been shown to affect mating preferences. They are therefore important candidates for the link between mate choice and indirect genetic benefits. Higher MHC diversity may be advantageous because this allows a wider range of pathogens to be detected and combated. Furthermore, individuals harbouring rare MHC alleles might better resist pathogen variants that have evolved to evade common MHC alleles. In the Seychelles warbler, females paired with low MHC‐diversity males elevate the MHC diversity of their offspring to levels comparable to the population mean by gaining extra‐pair fertilizations. Here, we investigate whether increased MHC diversity results in higher life expectancy and whether there are any additional benefits of extra‐pair fertilizations. Our 10‐year study found a positive association between MHC diversity and juvenile survival, but no additional survival advantage of extra‐pair fertilizations. In addition, offspring with a specific allele (Ase‐ua4) had a fivefold longer life expectancy than offspring without this allele. Consequently, the interacting effects of sexual selection and pathogen‐mediated viability selection appear to be important for maintaining MHC variation in the Seychelles warbler. Our study supports the prediction that MHC‐dependent extra‐pair fertilizations result in genetic benefits for offspring in natural populations. However, such genetic benefits might be hidden and not necessarily apparent in the widely used fitness comparison of extra‐ and within‐pair offspring.

Identifying the Critical Climatic Time Window That Affects Trait Expression

In cooperative breeders, the tension between the opposing forces of kin selection and kin competition is at its most severe. Although philopatry facilitates kin selection, it also increases the risk of inbreeding. When dispersal is limited, extra‐pair paternity might be an important mechanism to avoid inbreeding, but evidence for this is equivocal. The red‐winged fairy‐wren is part of a genus of cooperative breeders with extreme levels of promiscuity and male philopatry, but is unique in that females are also strongly philopatric. Here, we test the hypothesis that promiscuity is an important inbreeding avoidance mechanism when both sexes are philopatric. Levels of extra‐pair paternity were substantial (70% of broods), but did not arise through females mating with their helpers, but via extra‐group mating. Offspring were more likely to be sired by extra‐pair males when the social pair was closely related, and these extra‐pair males were genetically less similar to the female than the social male and thus, inbreeding is avoided through extra‐pair mating. Females were consistent in their choice of the extra‐pair sire over time and preferred early moulting males. Despite neighbouring males often being close kin, they sired 37% of extra‐pair offspring. However, females that gained paternity from neighbours were typically less related to them than females that gained paternity further away. Our study is the first to suggest that mating with both closely related social partners and neighbours is avoided. Such sophistication in inbreeding avoidance strategies is remarkable, as the extreme levels of promiscuity imply that social context may provide little cue to relatedness.

FLUCTUATING SELECTION AND THE MAINTENANCE OF INDIVIDUAL AND SEX-SPECIFIC DIET SPECIALIZATION IN FREE-LIVING OYSTERCATCHERS

Identifying the critical time window during which climatic drivers affect the expression of phenological, behavioral, and demographic traits is crucial for predicting the impact of climate change on trait and population dynamics. Two widely used associative methods exist to identify critical climatic periods: sliding-window models and recursive operators in which the memory of past weather fades over time. Both approaches have different strong points, which we combine here into a single method. Our method uses flexible functions to differentially weight past weather, which can reflect competing hypotheses about time lags and the relative importance of recent and past weather for trait expression. Using a 22-year data set, we illustrate that the climatic window identified by our new method explains more of the phenological variation in a sexually selected trait than existing approaches. Our new method thus helps to better identify the critical time window and the causes of trait response to environmental variability.

Identifying the best climatic predictors in ecology and evolution

Fluctuating and disruptive selection are important mechanisms for maintaining intrapopulation trait variation. Nonetheless, few field studies quantify selection pressures over long periods and identify what causes them to fluctuate. Diet specialists in oystercatchers differ in short‐term payoffs (intake), but their long‐term payoffs are hypothesized to be condition dependent. We test whether phenotypic selection on diet specialization fluctuates between years due to the frequency of specialists, competitor density, prey abundance, and environmental conditions. Short‐term payoffs proved to be poor predictors of long‐term fitness payoffs of specialization. Sex‐differences in diet specialization were maintained by opposing directional fecundity and viability selection between the sexes. Contrasting other studies, selection on individual diet specialization was neither negative frequency‐ or density‐dependent nor dependent on prey abundance. Notwithstanding, viability selection fluctuated strongly (stabilizing↔disruptive) over the 26‐year study period: slightly favoring generalists in most years, but strongly disfavoring generalists in rare harsh winters, suggesting generalists cannot cope with extreme conditions. Although selection fluctuated, mean selection on specialists was weak, which can explain how individual specialization can persist over long periods. Because rare events can dramatically affect long‐term selective landscapes, more care should be taken to match the timescale of evolutionary studies to the temporal variability of critical environmental conditions.

Behavioural, ecological and evolutionary responses to extreme climatic events: Challenges and directions

1.Ecologists and many evolutionary biologists relate variation in physiological, behavioral, life-history, demographic, population and community traits to variation in weather, a key environmental driver. However, identifying which weather variables (e.g. rain, temperature, El Nino index), over which time period (e.g. recent weather, spring or year-round weather) and in what ways (e.g. mean, threshold of temperature) they affect biological responses is by no means trivial, particularly when traits are expressed at different times among individuals. 2.A literature review shows that a systematic approach for identifying weather signals is lacking and that the majority of studies select weather variables from a small number of competing hypotheses that are founded on unverified a priori assumptions. This is worrying because studies that investigate the nature of weather signals in detail suggest that signals can be complex. Using suboptimal or wrongly-identified weather signals may lead to unreliable projections and management decisions. 3.We propose a four-step approach which allows for more rigorous identification and quantification of weather signals (or any other predictor variable for which data is available at high temporal resolution), easily implementable with our new R package ‘climwin’. We compare our approach with conventional approaches and provide worked examples. 4.Although our more exploratory approach also has some drawbacks–such as the risk of overfitting and bias that our simulations show can occur at low sample and effect sizes—these issues can be addressed with the right knowledge and tools. 5.By developing both the methods to fit critical weather windows to a wide range of biological responses and the tools to validate them and determine sample size requirements, our approach facilitates the exploration and quantification of the biological effects of weather in a rigorous, replicable, and comparable way, while also providing a benchmark performance to compare other approaches to.

Poor environmental tracking can make extinction risk insensitive to the colour of environmental noise.

More extreme climatic events (ECEs) are among the most prominent consequences of climate change. Despite a long-standing recognition of the importance of ECEs by paleo-ecologists and macro-evolutionary biologists, ECEs have only recently received a strong interest in the wider ecological and evolutionary community. However, as with many rapidly expanding fields, it lacks structure and cohesiveness, which strongly limits scientific progress. Furthermore, due to the descriptive and anecdotal nature of many ECE studies it is still unclear what the most relevant questions and long-term consequences are of ECEs. To improve synthesis, we first discuss ways to define ECEs that facilitate comparison among studies. We then argue that biologists should adhere to more rigorous attribution and mechanistic methods to assess ECE impacts. Subsequently, we discuss conceptual and methodological links with climatology and disturbance-, tipping point- and paleo-ecology. These research fields have close linkages with ECE research, but differ in the identity and/or the relative severity of environmental factors. By summarizing the contributions to this theme issue we draw parallels between behavioural, ecological and evolutionary ECE studies, and suggest that an overarching challenge is that most empirical and theoretical evidence points towards responses being highly idiosyncratic, and thus predictability being low. Finally, we suggest a roadmap based on the proposition that an increased focus on the mechanisms behind the biological response function will be crucial for increased understanding and predictability of the impacts of ECE. This article is part of the themed issue ‘Behavioural, ecological and evolutionary responses to extreme climatic events’.

Climatic conditions cause complex patterns of covariation between demographic traits in a long-lived raptor

The relative importance of environmental colour for extinction risk compared with other aspects of environmental noise (mean and interannual variability) is poorly understood. Such knowledge is currently relevant, as climate change can cause the mean, variability and temporal autocorrelation of environmental variables to change. Here, we predict that the extinction risk of a shorebird population increases with the colour of a key environmental variable: winter temperature. However, the effect is weak compared with the impact of changes in the mean and interannual variability of temperature. Extinction risk was largely insensitive to noise colour, because demographic rates are poor in tracking the colour of the environment. We show that three mechanisms—which probably act in many species—can cause poor environmental tracking: (i) demographic rates that depend nonlinearly on environmental variables filter the noise colour, (ii) demographic rates typically depend on several environmental signals that do not change colour synchronously, and (iii) demographic stochasticity whitens the colour of demographic rates at low population size. We argue that the common practice of assuming perfect environmental tracking may result in overemphasizing the importance of noise colour for extinction risk. Consequently, ignoring environmental autocorrelation in population viability analysis could be less problematic than generally thought.

Evolutionary origins and persistence of infidelity in Malurus: the least faithful birds

Environmental variation can induce life-history changes that can last over a large part of the lifetime of an organism. If multiple demographic traits are affected, expected changes in climate may influence environmental covariances among traits in a complex manner. Thus, examining the consequences of environmental fluctuations requires that individual information at multiple life stages is available, which is particularly challenging in long-lived species. Here, we analyse how variation in climatic conditions occurring in the year of hatching of female goshawks Accipiter gentilis (L.) affects age-specific variation in demographic traits and lifetime reproductive success (LRS). LRS decreased with increasing temperature in April in the year of hatching, due to lower breeding frequency and shorter reproductive life span. In contrast, the probability for a female to successfully breed was higher in years with a warm April, but lower LRS of the offspring in these years generated a negative covariance among fecundity rates among generations. The mechanism by which climatic conditions generated cohort effects was likely through influencing the quality of the breeding segment of the population in a given year, as the proportion of pigeons in the diet during the breeding period was positively related to annual and LRS, and the diet of adult females that hatched in warm years contained fewer pigeons. Climatic conditions experienced during different stages of individual life histories caused complex patterns of environmental covariance among demographic traits even across generations. Such environmental covariances may either buffer or amplify impacts of climate change on population growth, emphasizing the importance of considering demographic changes during the complete life history of individuals when predicting the effect of climatic change on population dynamics of long-lived species.