Barbara Tschirren

Proximate mechanisms of variation in the carotenoid-based plumage coloration of nestling great tits (Parus major L.).

Abstract Many vertebrates use carotenoid‐based signals in social or sexual interactions. Honest signalling via carotenoids implies some limitation of carotenoid‐based colour expression among phenotypes in the wild, and at least five limiting proximate mechanisms have been hypothesized. Limitation may arise by carotenoid‐availability, genetic constraints, body condition, parasites, or detrimental effects of carotenoids. An understanding of the relative importance of the five mechanisms is relevant in the context of natural and sexual selection acting on signal evolution. In an experimental field study with carotenoid supplementation, simultaneous cross‐fostering, manipulation of brood size and ectoparasite load, we investigated the relative importance of these mechanisms for the variation in carotenoid‐based coloration of nestling great tits (Parus major). Carotenoid‐based plumage coloration was significantly related to genetic origin of nestlings, and was enhanced both in carotenoid‐supplemented nestlings, and nestlings raised in reduced broods. We found a tendency for ectoparasite‐induced limitation of colour expression and no evidence for detrimental effects of carotenoids on growth pattern, mortality and recruitment of nestlings to the local breeding population. Thus, three of the five proposed mechanisms can generate individual variation in the expression of carotenoid‐based plumage coloration in the wild and thus could maintain honesty in a trait potentially used for signalling of individual quality.

Ectoparasite-modulated deposition of maternal androgens in great tit eggs.

Maternal yolk androgens can promote growth and competitive abilities of nestling birds but are also suggested to increase susceptibility to parasites or suppress immune function. We tested the hypothesis that females exposed to ectoparasites during egg formation will adjust the content of androgens in the yolk. We predicted that when anticipating high levels of parasitism, females deposit (i) less androgens into all eggs of their clutch and (ii) smaller amounts of androgens in eggs late in the laying sequence to facilitate brood reduction.In a field experiment we exposed female great tits (Parus major) to hen fleas (Ceratophyllus gallinae), or kept them free of ectoparasites prior to egg laying. We collected the eggs and measured yolk concentrations of androstenedione (A4), testosterone (T) and 5∝–dihydrotestosterone (DHT) by radioimmunoassay. Among clutches, eggs of ectoparasite–exposed females contained significantly less A4 and tended to contain less T, whereas DHT content was unaffected. Within clutches, content of A4 and T increased significantly with laying order whereas DHT content significantly decreased. These patterns were unaffected by ectoparasites. In summary, our results provide no evidence for hormone–based facilitation of brood reduction under ectoparasite exposure but support the hypothesis that females exposed to ectoparasites reduce levels of T and its precursor A4 in yolk and might thereby reduce the negative effects of parasites on offspring.

Short- and long-term consequences of early developmental conditions: a case study on wild and domesticated zebra finches

Divergent selection pressures among populations can result not only in significant differentiation in morphology, physiology and behaviour, but also in how these traits are related to each other, thereby driving the processes of local adaptation and speciation. In the Australian zebra finch, we investigated whether domesticated stock, bred in captivity over tens of generations, differ in their response to a life‐history manipulation, compared to birds taken directly from the wild. In a ‘common aviary’ experiment, we thereto experimentally manipulated the environmental conditions experienced by nestlings early in life by means of a brood size manipulation, and subsequently assessed its short‐ and long‐term consequences on growth, ornamentation, immune function and reproduction. As expected, we found that early environmental conditions had a marked effect on both short‐ and long‐term morphological and life‐history traits in all birds. However, although there were pronounced differences between wild and domesticated birds with respect to the absolute expression of many of these traits, which are indicative of the different selection pressures wild and domesticated birds were exposed to in the recent past, manipulated rearing conditions affected morphology and ornamentation of wild and domesticated finches in a very similar way. This suggests that despite significant differentiation between wild and domesticated birds, selection has not altered the relationships among traits. Thus, life‐history strategies and investment trade‐offs may be relatively stable and not easily altered by selection. This is a reassuring finding in the light of the widespread use of domesticated birds in studies of life‐history evolution and sexual selection, and suggests that adaptive explanations may be legitimate when referring to captive bird studies.

Maternal modulation of natal dispersal in a passerine bird: An adaptive strategy to cope with parasitism?

The decision of how far to disperse from the natal territory has profound and long‐lasting consequences for young animals, yet the optimal dispersal behavior often depends on environmental factors that are difficult or impossible to assess by inexperienced juveniles. Natural selection thus favors mechanisms that allow the adaptive and flexible adjustment of the offspring’s dispersal behavior by their parents via either paternal or maternal effects. Here we show that different dispersal strategies maximize the reproductive success of young great tits (Parus major) originating from a parasite‐infested or a parasite‐free nest and demonstrate that differential transfer of maternal yolk androgens in response to parasitism can result in a modification of the offspring’s dispersal behavior that appears adaptive. It demonstrates that prenatal maternal effects are an important yet so far neglected determinant of natal dispersal and highlights the potential importance of maternal effects in mediating coevolutionary processes in host‐parasite systems.

Parasites shape the optimal investment in immunity

The evolution of optimal functioning and maintenance of the immune system is thought to be driven by the costs arising from the allocation of resources to immune functions rather than to growth and reproduction and by the benefits arising from higher defence if an infection occurs. In young animals there is a high premium for fast growth and competitiveness and a parasite-mediated trade-off is thus predicted between the allocation of resources to growth versus immune function. In a field study on nestling great tits (Parus major), we manipulated simultaneously the level of immune defence by a dietary supplementation of the immunostimulant methionine and ectoparasite (Ceratophyllus gallinae) abundance in the nest and thereby assessed both the costs and benefits of investing in immune defence. Nestlings supplemented with methionine grew slower during the experimental boost of their immune system compared to controls. Thereafter, however, nestlings with a boosted immune system grew at faster rates under parasite pressure compared to unstimulated birds. It experimentally shows the costs and benefits of investment in immunity and suggests that the evolution of optimum host defence is governed by a parasite-mediated allocation trade-off between growth and immune function.

Carotenoid-based plumage colors and immune function: Is there a trade-off for rare carotenoids?

Theory suggests that carotenoid‐based signals are used in animal communication because they contain specific information about parasite resistance or immunocompetence. This implies that honesty of carotenoid‐based signals is maintained by a trade‐off between pigmentation and immune function for carotenoids, assuming that the carotenoids used for coloration are also immunoenhancing. We tested this hypothesis by altering the diets of nestling great tits (Parus major) with supplementary beadlets containing the carotenoids that are naturally ingested with food or beadlets containing the carotenoids that are incorporated into the feathers; a control group received beadlets containing no carotenoids. We simultaneously immune challenged half of the nestlings of each supplementation group, using a two‐factorial design. Activation of the immune system led to reduced color expression. However, only nestlings fed with the naturally ingested carotenoids and not with the carotenoids deposited in the feathers showed an increased cellular immune response. This shows that the carotenoids used for ornamentation do not promote the immune function, which conflicts with the trade‐off hypothesis. Our results indicate that honesty of carotenoid‐based signals is maintained by an individual’s physiological limitation to absorb and/or transport carotenoids and by access to carotenoids, indicating that preferences for carotenoid‐based traits in sexual selection or parent‐offspring interactions select for competitive individuals, rather than specifically for immune function.

Carotenoid-based colour expression is determined early in nestling life

Carotenoid-based colours are widespread in animals and are used as signals in intra- and interspecific communication. In nestling birds, the carotenoids used for feather pigmentation may derive via three pathways: (1) via maternal transfer to egg yolk; (2) via paternal feeds early after hatching when females are mainly brooding; or (3) via feeds from both parents later in nestling life. We analysed the relative importance of the proposed carotenoid sources in a field experiment on great tit nestlings (Parus major). In a within-brood design we supplemented nestlings with carotenoids shortly after hatching, later on in the nestling life, or with a placebo. We show that the carotenoid-based colour expression of nestlings is modified maximally during the first 6 days after hatching. It reveals that the observed variation in carotenoid-based coloration is based only on mechanisms acting during a short period of time in early nestling life. The experiment further suggests that paternally derived carotenoids are the most important determinants of nestling plumage colour.

Heritable variation in maternal yolk hormone transfer in a wild bird population

Differential reproductive investment by the mother can critically influence offspring development and phenotype, and strong selection is therefore expected to act on such maternal effects. Although a genetic basis is a prerequisite for phenotypic traits to respond to selection and thus to evolve, we still know very little about the extent of heritable variation in maternal effects in natural populations. Here, we present the first estimates of intrafemale repeatability across breeding seasons and estimates of heritability of hormone‐mediated maternal effects in a wild population of collared flycatchers (Ficedula albicollis). We found that maternal yolk testosterone (T) concentrations, yolk mass, and egg mass were moderately to highly repeatable within females across years, whereas intrafemale consistency of maternal yolk androstenedione (A4) deposition was low yet statistically significant. Furthermore, maternal yolk T transfer, yolk mass, and egg mass were significantly heritable, whereas yolk A4 transfer was not. These results strongly suggest that two major maternal yolk androgens are differentially regulated by genes and the environment. Selection on heritable variation in maternal yolk T deposition has the potential to shape the rate and direction of phenotypic change in offspring traits and can thereby accelerate or impede the response to selection in natural populations.

Carotenoid-based nestling colouration and parental favouritism in the great tit

While elaborate carotenoid-based traits in adult birds may have evolved as honest signals of individual quality in the context of sexual selection or other social interactions, the function of carotenoid-based colours in juveniles is less well understood. We investigated the hypothesis that carotenoid-based nestling colouration has evolved in response to parental preference of intensely coloured offspring during food provisioning. In a field experiment, we manipulated nestling plumage colouration by a carotenoid-supplementation and analysed the parental food provisioning behaviour before feather appearance and at the end of the nestling stage. Carotenoids per se did not influence the nestling’s begging behaviour or parental feeding decisions and we found no evidence that carotenoid-based colouration in nestling great tits has a signalling function in parent-offspring interactions. Parents did not discriminate between intensely coloured and control offspring in their food provisioning and in accordance with this finding intensely coloured nestlings were not heavier or larger at the end of the nestling stage. Alternative explanations for the evolution of carotenoid-based colours in nestling birds are discussed.

Evolutionary signals of selection on cognition from the great tit genome and methylome

For over 50 years, the great tit (Parus major) has been a model species for research in evolutionary, ecological and behavioural research; in particular, learning and cognition have been intensively studied. Here, to provide further insight into the molecular mechanisms behind these important traits, we de novo assemble a great tit reference genome and whole-genome re-sequence another 29 individuals from across Europe. We show an overrepresentation of genes related to neuronal functions, learning and cognition in regions under positive selection, as well as increased CpG methylation in these regions. In addition, great tit neuronal non-CpG methylation patterns are very similar to those observed in mammals, suggesting a universal role in neuronal epigenetic regulation which can affect learning-, memory- and experience-induced plasticity. The high-quality great tit genome assembly will play an instrumental role in furthering the integration of ecological, evolutionary, behavioural and genomic approaches in this model species.