Compatibility benefits of social and extra-pair mate choice in the zebra finch

Behavioural ecologists aim at providing insights into the
evolutionary and ecological processes that shape animal behaviour.
Mate choice is a decision faced by most animals that can strongly
affect an individual’s reproductive success, an important fitness
component. This behaviour has therefore the potential to show many
adaptations which have been the subject of a vivid research
interest over the last decades. Studies on mate choice have
typically focused on female preferences for traits that increase a
male's overall attractiveness, which supposedly reflects the male’s
absolute quality. Preferences for such traits are expected to
provide females with benefits such as good paternal care or ‘good
genes’ for their offspring. Nevertheless, in some species,
individuals actually show little consensus on what represents a
high-quality partner. Such individually-specific preferences are
poorly understood, but it has been hypothesized that they have
evolved to optimise genetic compatibility (to increase offspring
viability) or, although rarely mentioned, to optimise behavioural
compatibility (to facilitate joint parental care). The zebra finch
is a life-time monogamous passerine whose mating preferences for
putative quality traits have been widely studied but where no such
quality indicator has been repeatedly shown to influence mating
decisions. In this species, preferences seem instead largely
idiosyncratic. In this thesis, I investigated whether female zebra
finches choose genetically and/or behaviourally compatible social
mates (Chapters 2 and 3). More precisely, I measured, in a
large-scale breeding design, the fitness consequences of free mate
choice for compatibility while experimentally controlling for
effects of overall quality (Chapter 3). In this system, genetic
incompatibility results in embryo mortality and therefore hatching
failure, while behavioural incompatibility results in offspring
mortality. I therefore expected social mate choice for genetic
and/or behavioural compatibility to optimise embryo and offspring
survival (Chapter 3). Moreover, I tested whether siblings who grew
up together avoid choosing each other as social partner; in other
words, if they avoid inbreeding depression by choosing a
genetically more compatible partner (Chapter 2). In addition, I
performed a meta-analysis of published experiments on zebra finches
that allow for different mechanisms of kin discrimination to take
place (Chapter 2). Finally, I investigated whether females enhance
their extra-pair behaviour when paired to an apparently genetically
incompatible male to obtain compatible genes benefits (Chapter 1).
Indeed, extra-pair behaviour is largely hypothesized to be an
adaptive response that would allow females to compensate for a
potentially sub-optimal social mate choice. Specifically, I tested
whether female extra-pair mating evolved as a counter strategy when
females experience low hatching success with their social partner,
that is to say whether female extra-pair mate choice targets
fertility benefits and/or compatible genes benefits (Chapter 1).
Contrary to all expectations derived from optimality, zebra finches
were unable to identify partners with whom they would minimise
embryo mortality (Chapter 3), or to recognize unfamiliar kin on the
basis of genetic similarity per se to minimize inbreeding
depression (meta-analysis of Chapter 2), and did not adjust their
extra-pair mating behaviour in response to repeated hatching
failure (Chapter 1). This suggests that, in zebra finches,
individuals have not evolved any ability (other than avoiding
familiar kin, experiment of Chapter 2) to judge genetic
compatibility of any kind, despite the adaptive value of such
behaviour. Finally, allowing free social mate choice did enhance
pair fitness due to direct compatibility benefits (Chapter 3). This
thesis provides therefore the first evidence of mate choice for
behavioural compatibility. Nevertheless, the adaptive significance
of the underlying choosiness remains speculative (Chapter 3). A
null model consisting of random non-adaptive genetic variation in
sensory systems and variation in phenotypes that are better at
stimulating some sensory systems than others might well account for
the observed fitness differences between compatible and
incompatible pairs. This study highlights that there are limits to
adaptation.