Multi-level variation in labile characters

Labile characters, like behaviors, are phenotypes that are expressed repeatedly in the life of an individual. These types of characters allow individuals to adjust their phenotype to various levels of environmental variation, and therefore play a key role in the evolutionary process. Labile phenotypes are distinct because of their multi-level nature; individuals can differ in their average phenotypic expression (causing among-individual variation), but they can also vary their phenotype in each expression (causing within-individual variation). In order to understand the role of labile characters in the evolutionary process it is necessary to acknowledge that variation at each level is caused by different processes. Variation at the among-individual level is caused by genetic or environmental differences having a permanent effect on an individual’s phenotype, whereas variation at the within-individual level is caused by an individual’s adjustment of its phenotype to a changing environment. The implications of these multi layered effects in the expression of labile characters have been acknowledged by different fields of evolutionary ecology, but major areas of evolutionary research do not fully incorporated this idea. The general aim of my thesis was to fully integrate this multi-level nature in the study of the adaptive causes and evolutionary consequences of variation in labile characters. My thesis is composed of five chapters: the first three are conceptual and methodological works aimed at integrating the multi-level nature of labile characters into already existing evolutionary frameworks. The last two chapters describe, as a worked example, how the different levels of variation and covariation between (labile) fertilization related traits affect the evolution of the alternative reproductive strategies in a wild passerine bird (the great tit). The first chapter is a conceptual work focusing on how to define and statistically characterize behavioral characters. We argue that behavioral characters can be studied using the “evolutionary character concept”. This framework was developed to study characters that only vary among individuals (i.e. “fixed characters”); therefore we extended this framework to include characters that also vary within-individuals. The second chapter of the thesis is a methodological work where we proposed a way to quantify multi-level variation in reaction norms, which allows the estimation of repeatability of plasticity. Behavioral ecologists have recently developed theory predicting the ecological conditions where repeatable vs. non-repeatable variation in phenotypic plasticity should evolve. However, there was no methodological framework to estimate repeatability of plasticity. Therefore, we proposed a study design and mixed effect model structure to estimate repeatability of plasticity. To help researchers use the proposed methodology, we developed an R simulation package to estimate bias, precision and accuracy for different sampling designs. The third chapter is an opinion paper that urges researchers to combine theory and methods developed in behavioral ecology and quantitative genetics to study phenotypic variation in a social context. Quantitative geneticists have developed a framework to study social evolution aimed at predicting the evolutionary response to selection of traits affected by the phenotypes of other individuals (the “social environment”). Phenotypes expressed in a social context, also called interactive phenotypes, exhibit a particular evolutionary dynamic because their environmental component is composed of genes and can thus evolve. Despite that fact that the effects of the social environment are commonly mediated by labile characters, this social evolution framework has not fully considered the multi-level nature of labile characters. Therefore, for chapter three we integrated the multi-level nature of labile characters in this social evolution framework. The final two chapters focus, as a worked example, on within-pair and extra-pair reproductive behavior in great tits. For these chapters, we utilized the theoretical and methodological developments of the previous chapters to study the sources of evolutionary constraints on alternative fertilization routes in male great tits. One of the chapters has a more evolutionary perspective, while the other applies a more behavioral ecology view point. In chapter four we studied male extra-pair and within-pair reproduction as interactive phenotypes that are affected by the phenotypes of both the male and the female member of great tit breeding pairs. We showed that male fertilization strategies depend heavily on the phenotype of their female. This social environment effect should influence the evolutionary response to selection of male fertilization strategies, and could partly explain evolutionary stasis, observed in natural populations, in traits so closely linked to fitness. In chapter four we also studied whether trade-offs among- or within-individuals can constrain the phenotypic evolution of male alternative reproductive strategies. We showed that among-male trade-offs between within-pair and extra-pair reproduction could also be a source of evolutionary constrain. In chapter five, we corroborated the existence of trade-offs between alternative reproductive routes by studying whether within-pair and extra-pair fertilizations are obtained at the same time, allowing for the possibility of a trade-off between the two. We found that a male's extra-pair fertilization success is actually higher when it constrains his ability to secure within-pair fertilizations. This result is consistent with our finding that there is indeed a trade-off between extra-pair and within-pair reproduction in this species. The empirical works in this thesis highlight the importance of the social environment as a source of phenotypic variation in the expression of labile traits. But more generally, from the works in this thesis, we can conclude that to fully understand the role of labile characters in the evolutionary process it is necessary to acknowledge their multi-level nature

Multi-level variation in labile characters

Labile characters, like behaviors, are phenotypes that are expressed repeatedly in the life of an individual. These types of characters allow individuals to adjust their phenotype to various levels of environmental variation, and therefore play a key role in the evolutionary process. Labile phenotypes are distinct because of their multi-level nature; individuals can differ in their average phenotypic expression (causing among-individual variation), but they can also vary their phenotype in each expression (causing within-individual variation). In order to understand the role of labile characters in the evolutionary process it is necessary to acknowledge that variation at each level is caused by different processes. Variation at the among-individual level is caused by genetic or environmental differences having a permanent effect on an individual’s phenotype, whereas variation at the within-individual level is caused by an individual’s adjustment of its phenotype to a changing environment. The implications of these multi layered effects in the expression of labile characters have been acknowledged by different fields of evolutionary ecology, but major areas of evolutionary research do not fully incorporated this idea. The general aim of my thesis was to fully integrate this multi-level nature in the study of the adaptive causes and evolutionary consequences of variation in labile characters. My thesis is composed of five chapters: the first three are conceptual and methodological works aimed at integrating the multi-level nature of labile characters into already existing evolutionary frameworks. The last two chapters describe, as a worked example, how the different levels of variation and covariation between (labile) fertilization related traits affect the evolution of the alternative reproductive strategies in a wild passerine bird (the great tit). The first chapter is a conceptual work focusing on how to define and statistically characterize behavioral characters. We argue that behavioral characters can be studied using the “evolutionary character concept”. This framework was developed to study characters that only vary among individuals (i.e. “fixed characters”); therefore we extended this framework to include characters that also vary within-individuals. The second chapter of the thesis is a methodological work where we proposed a way to quantify multi-level variation in reaction norms, which allows the estimation of repeatability of plasticity. Behavioral ecologists have recently developed theory predicting the ecological conditions where repeatable vs. non-repeatable variation in phenotypic plasticity should evolve. However, there was no methodological framework to estimate repeatability of plasticity. Therefore, we proposed a study design and mixed effect model structure to estimate repeatability of plasticity. To help researchers use the proposed methodology, we developed an R simulation package to estimate bias, precision and accuracy for different sampling designs. The third chapter is an opinion paper that urges researchers to combine theory and methods developed in behavioral ecology and quantitative genetics to study phenotypic variation in a social context. Quantitative geneticists have developed a framework to study social evolution aimed at predicting the evolutionary response to selection of traits affected by the phenotypes of other individuals (the “social environment”). Phenotypes expressed in a social context, also called interactive phenotypes, exhibit a particular evolutionary dynamic because their environmental component is composed of genes and can thus evolve. Despite that fact that the effects of the social environment are commonly mediated by labile characters, this social evolution framework has not fully considered the multi-level nature of labile characters. Therefore, for chapter three we integrated the multi-level nature of labile characters in this social evolution framework. The final two chapters focus, as a worked example, on within-pair and extra-pair reproductive behavior in great tits. For these chapters, we utilized the theoretical and methodological developments of the previous chapters to study the sources of evolutionary constraints on alternative fertilization routes in male great tits. One of the chapters has a more evolutionary perspective, while the other applies a more behavioral ecology view point. In chapter four we studied male extra-pair and within-pair reproduction as interactive phenotypes that are affected by the phenotypes of both the male and the female member of great tit breeding pairs. We showed that male fertilization strategies depend heavily on the phenotype of their female. This social environment effect should influence the evolutionary response to selection of male fertilization strategies, and could partly explain evolutionary stasis, observed in natural populations, in traits so closely linked to fitness. In chapter four we also studied whether trade-offs among- or within-individuals can constrain the phenotypic evolution of male alternative reproductive strategies. We showed that among-male trade-offs between within-pair and extra-pair reproduction could also be a source of evolutionary constrain. In chapter five, we corroborated the existence of trade-offs between alternative reproductive routes by studying whether within-pair and extra-pair fertilizations are obtained at the same time, allowing for the possibility of a trade-off between the two. We found that a male's extra-pair fertilization success is actually higher when it constrains his ability to secure within-pair fertilizations. This result is consistent with our finding that there is indeed a trade-off between extra-pair and within-pair reproduction in this species. The empirical works in this thesis highlight the importance of the social environment as a source of phenotypic variation in the expression of labile traits. But more generally, from the works in this thesis, we can conclude that to fully understand the role of labile characters in the evolutionary process it is necessary to acknowledge their multi-level nature

Pathways to Social Evolution and Their Evolutionary Feedbacks

In the context of social evolution, the ecological drivers of selection are the phenotypes of other individuals. The social environment can thus evolve, potentially changing the adaptive value for different social strategies. Different branches of evolutionary biology have traditionally focused on different aspects of these feedbacks. Here, we synthesize behavioral ecology theory concerning evolutionarily stable strategies when fitness is frequency dependent with quantitative genetic models providing statistical descriptions of evolutionary responses to social selection. Using path analyses, we review how social interactions influence the strength of selection and how social responsiveness, social impact, and non-random social assortment affect responses to social selection. We then detail how the frequency-dependent nature of social interactions fits into this framework and how it imposes selection on traits mediating social responsiveness, social impact, and social assortment, further affecting evolutionary dynamics. Throughout, we discuss the parameters in quantitative genetics models of social evolution from a behavioral ecology perspective and identify their statistical counterparts in empirical studies. This integration of behavioral ecology and quantitative genetic perspectives should lead to greater clarity in the generation of hypotheses and more focused empirical research regarding evolutionary pathways and feedbacks inherent in specific social interactions

Personality traits differentially affect components of reproductive success in a Neotropical poison frog.

Individual reproductive success has several components, including the acquisition of mating partners, offspring production, and offspring survival until adulthood. While the effects of certain personality traits-such as boldness or aggressiveness-on single components of reproductive success are well studied, we know little about the composite and multifaceted effects behavioural traits can have on all the aspects of reproductive success. Behavioural traits positively linked to one component of reproductive success might not be beneficial for other components, and these effects may differ between sexes. We investigated the influence of boldness, aggressiveness, and exploration on the number of mating partners, mating events, and offspring surviving until adulthood in males and females of the Neotropical poison frog Allobates femoralis. Behavioural traits had different-even opposite-effects on distinct components of reproductive success in both males and females. For example, males who displayed high levels of aggressiveness and exploration (or low levels of aggressiveness and exploration) managed to attract high number of mating partners, while males with low levels of boldness, low levels of aggressiveness, and high levels of exploration had the most offspring surviving until adulthood. Our results therefore suggest correlational selection favouring particular combinations of behavioural traits

Most Published Selection Gradients Are Underestimated: Why This Is and How to Fix It

Ecologists and evolutionary biologists routinely estimate selection gradients. Most researchers seek to quantify selection on individual phenotypes, regardless of whether fixed or repeatedly expressed traits are studied. Selection gradients estimated to address such questions are attenuated unless analyses account for measurement error and biological sources of within-individual variation. Estimates of standardized selection gradients published in Evolution between 2010 and 2019 were primarily based on traits measured once (59% of 325 estimates). We show that those are attenuated: bias increases with decreasing repeatability but differently for linear versus nonlinear gradients. Others derived individual-mean trait values prior to analyses (41%), typically using few repeats per individual, which does not remove bias. We evaluated three solutions, all requiring repeated measures: (i) correcting gradients derived from classic models using estimates of trait correlations and repeatabilities, (ii) multivariate mixed-effects models, previously used for estimating linear gradients (seven estimates, 2%), which we expand to nonlinear analyses, and (iii) errors-in-variables models that account for within-individual variance, and are rarely used in selection studies. All approaches produced accurate estimates regardless of repeatability and type of gradient, however, errors-in-variables models produced more precise estimates and may thus be preferable

A statistical methodology for estimating assortative mating for phenotypic traits that are labile or measured with error

Assortative mating in wild populations is commonly reported as the correlation between males’ and females’ phenotypes across mated pairs. Theories of partner selection and quantitative genetics assume that phenotypic resemblance of partners captures associations in “intrinsically determined” trait values. However, when considering traits with a repeatability below one (labile traits or traits measured with error), the correlation between phenotypes of paired individuals can arise from shared environmental effects on the phenotypes of paired individuals or correlated measurement error.We introduce statistical approaches to estimate assortative mating in labile traits or traits measured with error in the presence of shared environmental effects. These approaches include (1) the correlation between the mean phenotypes of males and females, (2) the correlation between randomized values of individuals and (3) the between-pair correlation derived from a bivariate mixed model.We use simulations to show that the performance of these different approaches depends on the number of repeated measures within individuals or pairs, which is determined by study design, and rates of survival and divorce.We conclude that short-term environmental effects on phenotypes of paired individuals likely inflate estimates of assortative mating when not statistically accounted for. Our approach allows investigation of this important issue in assortative mating studies for labile traits (e.g. behaviour, physiology, or metabolism) in both socially monogamous and other mating systems, and groupings of individuals outside a mating context.</ol

Long‐distance dispersal in the short‐distance dispersing house sparrow ( Passer domesticus )

The house sparrow (Passer domesticus) is a small passerine known to be highly sedentary. Throughout a 30‐year capture–mark–recapture study, we have obtained occasional reports of recoveries far outside our main metapopulation study system, documenting unusually long dispersal distances. Our records constitute the highest occurrence of long‐distance dispersal events recorded for this species in Scandinavia. Such long‐distance dispersals radically change the predicted distribution of dispersal distances and connectedness for our study metapopulation. Moreover, it reveals a much greater potential for colonization than formerly recorded for the house sparrow, which is an invasive species across four continents. These rare and occasional long‐distance dispersal events are challenging to document but may have important implications for the genetic composition of small and isolated populations and for our understanding of dispersal ecology and evolution

Longitudinal telomere dynamics within natural lifespans of a wild bird

Telomeres, the nucleotide sequences that protect the ends of eukaryotic chromosomes, shorten with each cell division and telomere loss may be influenced by environmental factors. Telomere length (TL) decreases with age in several species, but little is known about the sources of genetic and environmental variation in the change in TL (∆TL) in wild animals. In this study, we tracked changes in TL throughout the natural lifespan (from a few months to almost 9 years) of free-living house sparrows (Passer domesticus) in two different island populations. TL was measured in nestlings and subsequently up to four times during their lifetime. TL generally decreased with age (senescence), but we also observed instances of telomere lengthening within individuals. We found some evidence for selective disappearance of individuals with shorter telomeres through life. Early-life TL positively predicted later-life TL, but the within-individual repeatability in TL was low (9.2%). Using genetic pedigrees, we found a moderate heritability of ∆TL (h2 = 0.21), which was higher than the heritabilities of early-life TL (h2 = 0.14) and later-life TL measurements (h2 = 0.15). Cohort effects explained considerable proportions of variation in early-life TL (60%), later-life TL (53%), and ∆TL (37%), which suggests persistent impacts of the early-life environment on lifelong telomere dynamics. Individual changes in TL were independent of early-life TL. Finally, there was weak evidence for population differences in ∆TL that may be linked to ecological differences in habitat types. Combined, our results show that individual telomere biology is highly dynamic and influenced by both genetic and environmental variation in natural conditions