The evolution of reproductive isolation between populations by divergent natural selection commonly drives the origin of species (Schluter 2001). Many studies attempt to infer evolutionary processes from current differences in genetic, vocal, morphological, ecological, and behavioral traits (Coyne and Orr 2004). In an integrative approach, this study aims to determine the relative contributions and interplay of all these traits leading to population divergence, thus contributing to the development of our understanding of evolution. In particular, I focus on ecological speciation, the divergence by local adaptation to different environments in birds. Within the concept of ecological speciation, the local adaptation hypothesis predicts that birds which select mates from their natal regions will gain fitness advantages because their offspring will more likely express adaptations to local ecological conditions (Kawecki and Ebert 2004). Benefits of local adaptation contrast with potential disadvantages such as inbreeding, which is generally avoided through dispersal. According to the local adaptation hypothesis, these disadvantages are outweighed by the benefits of selecting local mates. However, although ecological conditions may induce natural selection for local adaptation, disruptive or diversifying selection is generally not sufficient for speciation if individuals can migrate between populations. In this case, a mating system has to emerge that strongly reduces gene flow between ecologically diverging populations (Coyne and Orr 2004).
In this thesis, I am particularly interested in natural and sexual selection related to the role of seasonality, and in behavior (song) and physiology (hormones) that play important roles in adaptation to seasonal environments (Helm et al. 2009; Baldwin et al. 2010).
S ong
Surprisingly, only very little is known about whether and how interactions of natural and sexual selection facilitate or constrain speciation (reviewed in (Maan and Seehausen 2011)). Biologists often either consider sexual selection in isolation from natural selection, or address ecological effects on sexually selected traits, but rarely assess the implications for population divergence. In this study, I aim to integrate several components of potential speciation-facilitating mechanisms focusing on both, natural and sexual selection with emphasis on the effects of seasonality and song, respectively, and their interactions on population divergence. Hereby, I make inferences about the dynamics of genetic differentiation using sophisticated statistical landscape genetics. Adaptive traits favored by environmental factors may support diversification that emerges from interactions between sexual selection and environmental heterogeneity (reviewed in (Maan and Seehausen 2011)). Phenotypic
traits involved in signaling, for example aspects of song and morphology, have been identified to contribute to reproductive isolation between diverging populations (Marler 1957; Coyne and Orr 2004). Specifically, signaling in the context of resource defense or mate attraction may enhance reproductive isolation through assortative mating (Grant and Grant 2002; Edwards et al. 2005; Price and Sol 2008; Podos 2010). In many songbirds, songs are a key component of signaling and are transmitted across generations via vocal learning (Slabbekoorn and Smith 2002). Accordingly, song dialects, i.e. the unique repertoire of shared songs within a population, combined with female preference for a local dialect due to parental imprinting, may lead to reproductive divergence (Marler and Tamura 1962; Nottebohm 1969; Baker 1975; Searcy 1992).
The relationship between local adaptation and associated signaling on the one hand, and female preference on the other, can also be affected by a species’ life history (Helbig 2003). In particular, avian migration may counteract reproductive divergence (Paradis et al. 1998; Nelson 1999; Helbig 2003) because migrants are typically under time pressure to make rapid reproductive decisions (Reed et al.
1999), and may therefore not pair with the most advantageous, locally adapted mate available (Randler 2002). Moreover, in migratory birds, individuals of higher phenotypic quality are often observed to arrive and mate first (Francis and Cooke 1988; Lundberg and Alatalo 1992; Møller 1994; Lozano et al.
1995). This phenomenon is commonly explained by the reasoning that birds with advanced seasonal reproductive timing may gain the best territories, but only high quality males will be able to survive the costs associated with early arrival (Kokko 1999).
S easonality
Successful breeding requires that birds closely match their breeding period, and thus their reproductive behavior with the often brief moment when environmental conditions are favorable (Prestt 1971; Murton and Westwood 1977). Temporal shifts in life history stages towards favorable environmental conditions, for example through increased abundance of resources, are thus likely to foster survival and reproductive success (Durant et al. 2007). Under these circumstances, the adaptation to diversifying seasonal environments may promote such phenotypic divergence between populations even more rapidly. Because seasonal activities must be accurately timed to avoid mismatches with the environment (Bradshaw and Holzapfel 2007), some animals have rigid circannual rhythms, i.e. endogenously generated biological rhythms of approximately one year. This has the advantage of regulating timing under a suite of conditions and of buffering organisms from responding to misleading, random environmental variability (Hahn et al. 1997). The timing of reproduction is considered as one of the major life history traits reflecting the adaptation of birds to local features of their environment (Visser and Lambrechts 1999). This pattern of local adaptation to the seasonality of the environment has striking implications on a larger geographical scale. Organisms
tend to cluster along a latitudinal gradient associated with differences in their life histories, the pace of life axis. In the northern hemisphere, temperate zone birds are relatively short-lived and produce a high number of offspring, which develop relatively fast and mature early in life, the fast end of the life-history axis, whereas tropical birds lie at the opposite end of this continuum (Wiersma et al. 2007).
A major aim of this study is to understand the contributions of these adaptive temporal patterns in avian life histories to evolution. In addition to environmental seasonality and song, this includes an interest in the underlying endocrine regulations.
H ormones
The physiological and behavioral mechanisms that lead to life history trade-offs are often under endocrine regulation (Stearns 1989). Testosterone is one physiological factor proposed to mediate the trade-off between reproduction and survival (reviewed in (Hau 2007)). In particular, it has important pleiotropic effects on resource allocation for mate attraction, competitive behavior, reproductive effort, and associated signal plasticity, while often simultaneously decreasing fitness by suppressing traits such as immune function and parental care. Therefore, seasonal peaks in testosterone can be brief and typically coincide with periods of intense competition between males for territories and mating partners. This study aims to determine the time patterns of testosterone production in a seasonally changing environment, and the diverse effects it has on song, physiology and behavior.
Environmentally induced phenotypic variation allows developing organisms to respond adaptively to changes in their environment, and can directly alter an individual’s behavior, morphology and physiology. On a large scale, this phenotypic variation in testosterone levels seems to follow a latitudinal trend along the pace of life axis. Tropical birds tend to have lower testosterone levels (Garamszegi et al. 2008) and seem to lack a peak in testosterone at the beginning of the breeding season (Wikelski et al. 2003a; Onofrei et al. 2004) compared to species breeding at higher latitudes. In a comparative approach along the pace of life axis, I aim to test if testosterone may act as a proximate mediator of latitudinal phenotypic and behavioral variation within the Stonechat complex, a study species with well-known life history traits. For a more detailed examination of the associations of seasonality, song and the hormonal regulation in the context of territoriality, I studied the Black redstarts, Phoenicurus ochruros, during distinct life cycle stages.