Mathias Kölliker

Immunocompetence of nestling great tits in relation to rearing environment and parentage

Theoretical models of host–parasite coevolution assume a partially genetic basis to the variability in susceptibility to parasites among hosts, for instance as a result of genetic variation in immune function. However, few empirical data exist for free–living vertebrate hosts to support this presumption. In a cross–fostering experiment with nestling great tits, by comparing nestlings of the same origin we investigated (i) the variance in host resistance against an ectoparasite due to a common genetic origin, (ii) the effect of ectoparasite infestation on cell–mediated immunity and (iii) the variance in cell–mediated immunity due to a common genetic origin. Ectoparasitic hen fleas can impair the growth of nestling great tits and nestling growth was therefore taken as a measure of host susceptibility. A common origin did not account for a significant part of the variation in host susceptibility to fleas. There was no significant overall effect of fleas on nestling growth or cell–mediated immunity, as assessed by a cutaneous hypersensitivity response. A common rearing environment explained a significant part of the variation in cell–mediated immunity among nestlings, mainly through its effect on nestling body mass. The variation in cell–mediated immunity was also related to a common origin. However, the origin–related variation in body mass did not account for the origin–related differences in cell–mediated immunity. The results of the present study thus suggest heritable variation in cell–mediated immunity among nestling great tits.

The quantitative genetic basis of offspring solicitation and parental response in a passerine bird with biparental care

The coevolution of parental investment and offspring solicitation is driven by partly different evolutionary interests of genes expressed in parents and their offspring. In species with biparental care, the outcome of this conflict may be influenced by the sexual conflict over parental investment. Models for the resolution of such family conflicts have made so far untested assumptions about genetic variation and covariation in the parental resource provisioning response and the level of offspring solicitation. Using a combination of cross-fostering and begging playback experiments, we show that, in the great tit (Parus major), (i) the begging call intensity of nestlings depends on their common origin, suggesting genetic variation for this begging display, (ii) only mothers respond to begging calls by increased food provisioning, and (iii) the size of the parental response is positively related to the begging call intensity of nestlings in the maternal but not paternal line. This study indicates that genetic covariation, its differential expression in the maternal and paternal lines and/or early environmental and parental effects need to be taken into account when predicting the phenotypic outcome of the conflict over investment between genes expressed in each parent and the offspring.

Benefits of Induced Host Responses against an Ectoparasite

As a consequence of the deleterious effects of parasites on host fitness, hosts have evolved responses to minimize the negative impact of parasite infection. Facultative parasite–induced responses are favoured when the risk of infection is unpredictable and host responses are costly. In vertebrates, induced responses are generally viewed as being adaptive, although evidence for fitness benefits arising from these responses in natural host populations is lacking. Here we provide experimental evidence for direct reproductive benefits in flea–infested great tit nests arising from exposure during egg production to fleas. In the experiment we exposed a group of birds to fleas during egg laying (the exposed group), thereby allowing for induced responses, and kept another group free of parasites (the unexposed group) over the same time period. At the start of incubation, we killed the parasites in both groups and all nests were reinfested with fleas. If induced responses occur and are adaptive, we expect that birds of the exposed group mount earlier responses and achieve higher current reproductive success than birds in the unexposed group. In agreement with this prediction, our results show that birds with nests infested during egg laying have (i) fewer breeding failures and raise a higher proportion of hatchlings to fledging age; (ii) offspring that reach greater body mass, grow longer feathers, and fledge earlier, and (iii) a higher number of recruits and first–year grandchildren than unexposed birds. Flea reproduction and survival did not differ significantly between the two treatments. These results provide the first evidence for the occurrence and the adaptiveness of induced responses against a common ectoparasite in a wild population of vertebrates.

Parent-offspring conflict and co-adaptation: behavioural ecology meets quantitative genetics

The evolution of the complex and dynamic behavioural interactions between caring parents and their dependent offspring is a major area of research in behavioural ecology and quantitative genetics. While behavioural ecologists examine the evolution of interactions between parents and offspring in the light of parent–offspring conflict and its resolution, quantitative geneticists explore the evolution of such interactions in the light of parent–offspring co-adaptation due to combined effects of parental and offspring behaviours on fitness. To date, there is little interaction or integration between these two fields. Here, we first review the merits and limitations of each of these two approaches and show that they provide important complementary insights into the evolution of strategies for offspring begging and parental resource provisioning. We then outline how central ideas from behavioural ecology and quantitative genetics can be combined within a framework based on the concept of behavioural reaction norms, which provides a common basis for behavioural ecologists and quantitative geneticists to study the evolution of parent–offspring interactions. Finally, we discuss how the behavioural reaction norm approach can be used to advance our understanding of parent–offspring conflict by combining information about the genetic basis of traits from quantitative genetics with key insights regarding the adaptive function and dynamic nature of parental and offspring behaviours from behavioural ecology.

Bird-ectoparasite interactions, nest humidity, and ectoparasite community structure

Host nests are the key habitat for ectoparasite species that live and reproduce within the nest material. Nest properties can influence host and parasite reproductive success, and therefore the outcome of host–parasite interactions, as well as the composition of parasite communities. Previous correlational results suggested that nest humidity may increase the negative effect of fleas on Great Tit (Parus major) reproductive success. Since the causality of the relationship was unknown, we simultaneously manipulated both hen flea (Ceratophyllus gallinae) infestation and nest humidity in order to investigate: (1) the effect of flea infestation on nest humidity, (2) the effect of nest humidity on the prevalence of flea infestations, (3) the effect of nest humidity on adult flea survival and reproduction, (4) the interaction between flea infestations and nest humidity on Great Tit reproductive performance, and (5) the effect of both factors on secondary infestations by ectoparasitic Protocalliphora flies. The p...

Benefits and costs of earwig (Forficula auricularia) family life

The evolution of parental care and family group formation critically depends on offspring survival benefits and parental fecundity costs of care under given ecological conditions. Investigations of the functional significance of care in insect species that exhibit facultative parental care have been relatively rare but may be of particular interest for better understanding of benefit and cost schedules at an early evolutionary stage. In this study, aspects of benefits and costs of care were addressed in the sub-social European earwig (Forficula auricularia; Dermaptera: Forficulidae) by manipulating the presence of tending mothers and brood size in a fully crossed experimental design. Larvae growing in broods tended by their mother or of reduced size showed a higher survival probability than larvae growing in untended or large broods, as predicted if maternal care is beneficial and shaped by a trade-off between number and quality of offspring. Analysis of patterns of food consumption and developmental time further suggested that the benefit of maternal attendance is mediated by the maternal provisioning of food, while the quality–quantity trade-off seemed to be driven by sibling rivalry. Further, tending mothers delayed the production of a second clutch, indicating a potential cost of care in terms of lifetime fecundity. This study experimentally shows benefits and potential costs of maternal care and family group formation in the European earwig. More detailed behavioural experiments will be required to fully understand how behavioural interactions among family members mediate these reproductive outcomes.

Ectoparasite infestation and sex-biased local recruitment of hosts

Dispersal patterns of organisms are a fundamental aspect of their ecology, modifying the genetic and social structure of local populations,,,. Parasites reduce the reproductive success and survival of hosts and thereby exert selection pressure on host life-history traits,,, possibly affecting host dispersal,,. Here we test experimentally whether infestation by hen fleas, Ceratophyllus gallinae, affects sex-related recruitment of great tit, Parus major, fledglings. Using sex-specific DNA markers, we show that flea infestation led to a higher proportion of male fledglings recruiting in the local population in one year. In infested broods, the proportion of male recruits increased with brood size over a three year period, whereas the proportion of male recruits from uninfested broods decreased with brood size. Natal dispersal distances of recruits from infested nests were shorter than those from uninfested nests. To our knowledge, this study provides the first evidence for parasite-mediated host natal dispersal and local recruitment in relation to sex. Current theory needs to consider parasites as potentially important factors shaping life-history traits associated with host dispersal.

A chemical signal of offspring quality affects maternal care in a social insect

Begging signals of offspring are condition-dependent cues that are usually predicted to display information about the short-term need (i.e. hunger) to which parents respond by allocating more food. However, recent models and experiments have revealed that parents, depending on the species and context, may respond to signals of quality (i.e. offspring reproductive value) rather than need. Despite the critical importance of this distinction for life history and conflict resolution theory, there is still limited knowledge of alternative functions of offspring signals. In this study, we investigated the communication between offspring and caring females of the common earwig, Forficula auricularia, hypothesizing that offspring chemical cues display information about nutritional condition to which females respond in terms of maternal food provisioning. Consistent with the prediction for a signal of quality we found that mothers exposed to chemical cues from well-fed nymphs foraged significantly more and allocated food to more nymphs compared with females exposed to solvent (control) or chemical cues from poorly fed nymphs. Chemical analysis revealed significant differences in the relative quantities of specific cuticular hydrocarbon compounds between treatments. To our knowledge, this study demonstrates for the first time that an offspring chemical signal reflects nutritional quality and influences maternal care.

The evolution of parental care in insects: the roles of ecology, life history and the social environment

Parental care increases the fitness of offspring at a cost to the parents in terms of residual reproductive success. This trade‐off may be affected by ecology, life history and the social environment, which raises the question as to how these factors contribute to the evolution of parental care. Here, previous hypotheses concerning the evolution of parental care in insects are summarized and discussed and the underlying empirical evidence is reviewed. Ecological factors such as harsh environments, ephemeral food sources or predation pressure are broadly accepted as evolutionary drivers of parental care. The most consistent evidence supports a role for natural enemies such as predators, microbes and cannibalistic conspecifics. Also, the importance of ecological factors may interact with the life history (parity) of a species, either as a pre‐adaptation facilitating the evolution of parental care or as a consequence of enhanced parental investment under parental care. Yet, only limited experimental research has been carried out to test the combined influence of ecology and life history in the evolution of parental care. Several forms of care can mediate the transition from solitary to family living, which entails the emergence of a novel – social – environment that generates new selection pressures from interactions within and between families. In this context, we review examples of studies on communal breeding, brood parasitism, parent–offspring conflict and co‐adaptation, and discuss how these social interactions may in turn be influenced by ecological factors such as food availability or population density. Insects are uniquely suitable for experimental and comparative research on the complex interplay between ecology, life history, and the social environment.

EFFECTS OF COMMON ORIGIN AND COMMON ENVIRONMENT ON NESTLING PLUMAGE COLORATION IN THE GREAT TIT (PARUS MAJOR)

Abstract.— Carotenoids cannot be synthesized by birds and thus have to be ingested with food, suggesting that ca‐rotenoid‐based plumage coloration is environmentally determined. However signaling functions ascribed to plumage imply that plumage coloration is the outcome of an evolutionary process based on genetic variation. By means of a cross‐fostering design we show significant effects of both a common rearing environment and the brood from which a nestling originally came from (common origin) on the plumage coloration of nestling great tits (Parus major). This demonstration of origin‐related variation in carotenoid‐based plumage coloration suggests that the observed variation of the trait has a partial genetic basis. Consistent with environmental determination of this trait, we also found a significant positive correlation between the color saturation of nestlings and their foster‐fathers plumage. There was no significant correlation between nestling plumage coloration and the food quantity provided to the nestlings by the male, the female, or both parents. This suggests that the nestling‐foster father correlation arises by the carotenoid quantity ingested rather than the food quantity per se. No significant nestling‐true father correlation was found, which suggests that nestling plumage coloration did not indirectly evolve due to sexual selection. Consistent with this result there was no significant correlation between the nestlings plumage color and its coloration as a breeding adult the following year, suggesting that nestling plumage color is a different trait than the first year plumage.