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.