Wolfgang Winkel

PATERNAL GENETIC EFFECTS ON OFFSPRING FITNESS ARE CONTEXT DEPENDENT WITHIN THE EXTRAPAIR MATING SYSTEM OF A SOCIALLY MONOGAMOUS PASSERINE

Abstract Avian extrapair mating systems provide an interesting model to assess the role of genetic benefits in the evolution of female multiple mating behavior, as potentially confounding nongenetic benefits of extrapair mate choice are seen to be of minor importance. Genetic benefit models of extrapair mating behavior predict that females engage in extrapair copulations with males of higher genetic quality compared to their social mates, thereby improving offspring reproductive value. The most straightforward test of such good genes models of extrapair mating implies pairwise comparisons of maternal half‐siblings raised in the same environment, which permits direct assessment of paternal genetic effects on offspring traits. But genetic benefits of mate choice may be difficult to detect. Furthermore, the extent of genetic benefits (in terms of increased offspring viability or fecundity) may depend on the environmental context such that the proposed differences between extrapair offspring (EPO) and within‐pair offspring (WPO) only appear under comparatively poor environmental conditions. We tested the hypothesis that genetic benefits of female extrapair mate choice are context dependent by analyzing offspring fitness‐related traits in the coal tit (Parus ater) in relation to seasonal variation in environmental conditions. Paternal genetic effects on offspring fitness were context dependent, as shown by a significant interaction effect of differential paternal genetic contribution and offspring hatching date. EPO showed a higher local recruitment probability than their maternal half‐siblings if born comparatively late in the season (i.e., when overall performance had significantly declined), while WPO performed better early in the season. The same general pattern of context dependence was evident when using the number of grandchildren born to a cuckolding female via her female WPO or EPO progeny as the respective fitness measure. However, we were unable to demonstrate that cuckolding females obtained a general genetic fitness benefit from extrapair fertilizations in terms of offspring viability or fecundity. Thus, another type of benefit could be responsible for maintaining female extrapair mating preferences in the study population. Our results suggest that more than a single selective pressure may have shaped the evolution of female extrapair mating behavior in socially monogamous passerines.

Polygynie des Trauerschnäppers(Ficedula hypoleuca) am Westrand seines Areals in Mitteleuropa

1974–1983 waren in einem mit 600 künstlichen Nisthöhlen ausgestatteten Lärchen-Versuchsforst (52.27 N, 7.15 E) bei Lingen/Emsland beim Trauerschnäpper 20,7% der ♀ nachweislich mit einem polygamen ♂ verpaart. Neben 51 Bigynie-Fällen konnte auch 4mal Trigynie nachgewiesen werden. ♂ mit Polygamie-Nachweis waren im Mittel älter als die übrigen ♂ (2,71 bzw. 2,18 Jahre). Polygame ♂ hatten im Durchschnitt längere Flügel und ein größeres Gewicht als ♂ ohne Polygamie-Nachweis, was als Folge der unterschiedlichen Altersstruktur zu deuten ist. Brutkästen der Bigamisten waren im Mittel 258 m voneinander entfernt (Maximum 750 m). Bei Bruten ohne Nachweis eines fütternden ♂ lag die Anzahl ausgeflogener Junge (im Mittel 2,9) gesichert unter dem Bruterfolg von zwei anderen Gruppen (fütterndes ♂ bei einer Brut festgestellt 4,7; fütterndes ♂ bei 2–3 Bruten festgestellt 4,5). Zwischen den Schlüpfterminen von Bigamisten-Bruten lagen 1–16

Polygyny and its fitness consequences for primary and secondary female pied flycatchers

(\bar x = 7)

Genetic similarity between pair mates is not related to extrapair paternity in the socially monogamous coal tit

Tage. Das Durchschnittsalter der ♀ in den jeweils früheren Bruten betrug 2,67, in den jeweils späteren Bruten 1,67 Jahre. 1974–1983 in a study area of larch forest (52.27 N, 7.15 E), with 600 nestboxes, near Lingen/Emsland in western Lower Saxony, polygyny among Pied Flycatchers was identified as participation of ♂ in feeding at 2 or 3 nestboxes (bigyny or trigyny). 20.7% of ♀ were shown to be paired with a polygamous ♂. Beside 51 cases of bigyny 4 cases of trigyny were identified. The incidence of polygyny was also considered in relation to the „border situation“ of the study area. Proven polygamous ♂ were on average older than other ♂ (2.71 as compared to 2.18 years). On average polygamous ♂ had longer wings and greater bodyweight than ♂ without polygamous record, which is to be interpreted as a result of differing age structure. On average the mean distance between nestboxes of bigamists was 258 m (max. 750 m). In cases of broods without recorded feeding ♂ (generally this would occur in cases of secondary broods of polygamous ♂ in which the ♂ assisted only rarely or not at all) the number of reared young (on average 2.9) was significantly lower than the breeding success realised by 2 other groups (♂ recorded as assisting in rearing one brood only 4.7; ♂ recorded as assisting in rearing 2–3 broods 4.5). A period of 1–16 days (on average 7) elapsed between the hatching dates of broods of bigamists. The average age of ♀ in the earlier broods was 2.67 yrs, in the later broods 1.67 yrs.

Zum Ortstreue-Verhalten des Trauerschnäppers(Ficedula hypoleuca) im westlichen Randbereich seines mitteleuropäischen Verbreitungsgebietes

Females of many socially monogamous bird species commonly engage in extra-pair copulations. Assuming that extra-pair males are more attractive than the females’ social partners and that attractiveness has a heritable component, sex allocation theory predicts facultative overproduction of sons among extra-pair offspring (EPO) as sons benefit more than daughters from inheriting their father’s attractiveness traits. Here, we present a large-scale, three-year study on sex ratio variation in a passerine bird, the coal tit (Parus ater). Molecular sexing in combination with paternity analysis revealed no evidence for a male-bias in EPO sex ratios compared to their within-pair maternal half-siblings. Our main conclusion, therefore, is that facultative sex allocation to EPO is absent in the coal tit, in accordance with findings in several other species. Either there is no net selection for a deviation from random sex ratio variation (e.g. because extra-pair mating may serve goals different from striving for ‘attractiveness genes’) or evolutionary constraints preclude the evolution of precise maternal sex ratio adjustment. It is interesting to note that, however, we found broods without EPO as well as broods without mortality to be relatively female-biased compared to broods with EPO and mortality, respectively. We were unable to identify any environmental or parental variable to co-vary with brood sex ratios. There was no significant repeatability of sex ratios in consecutive broods of individual females that would hint at some idiosyncratic maternal sex ratio adjustment. Further research is needed to resolve the biological significance of the correlation between brood sex ratios and extra-pair paternity and mortality incidence, respectively.

Über die brutzeitliche Gewichtsentwicklung beim Trauerschnäpper(Ficedula hypoleuca)

In polygynous species with biparental care, the amount of paternal support often varies considerably. In the pied flycatcher (Ficedula hypoleuca), females mated with monogamous males receive more male assistance during the nestling phase than females mated with bigynous males, as the latter have to share their mates with another female. Bigynous males, however, give more support to their primary broods than to their secondary broods. Using a long-term dataset (31 years), the present study revealed that direct reproductive success, i.e. number of fledglings, was lower in females that mated with bigynous males, especially in secondary broods without male assistance, than in females that mated with monogamous males. Secondary broods with male assistance were more affected than primary broods. Female survival was independent of mating status. In primary broods, a delayed compensation for inferior direct reproductive success was found in terms of the number of grandoffspring, a phenomenon that did not occur in secondary broods. Delayed compensation in primary broods refers to indirect effects, i.e. good genes. According to the sexy son hypothesis, genetically superior (i.e. sexy) males may have sons with a higher number of broods belonging to a polygynous breeding status than do sons from broods with a monogamous father. This was indeed the case for sons descending from primary broods, but not for sons descending from secondary broods.

Zur Populationsdynamik der Blaumeise (Parus caeruleus): Langfristige Studien bei Braunschweig

Für den Komplex des Umwelt-Faktorengefüges, das für die Existenz einer Art notwendig ist, wird aus autökologischer Sicht der Begriff „Ökoschema“ und als Überbegriff für Konkurrenz (um ein begrenzt vorhandenes Requisit) und Interferenz (als direkte Konfrontation) der Ausdruck „Rivalität“ vorgeschlagen und verwendet. Unter „Dismigration“ sind sämtliche aktiven Ortsbewegungen zu verstehen, die zu einer Änderung der „Dispersion“ (als Zustand der Individuenverteilung im Raum) führen. Die genannten „öko-ethologischen“ Dispersionsfaktoren sind dadurch gekennzeichnet, daß in ihnen sowohl Umweltgegebenheiten als auch Verhaltensweisen zusammenwirken. In der vorliegenden Arbeit wird untersucht, welchen Einfluß die öko-ethologischen Faktoren Ökoschema, Rivalität und Dismigration auf die Dispersion der Individuen in einer Population ausüben. Anhand der Ergebnisse werden die folgenden drei öko-ethologischen Dispersions-Grundsätze aufgestellt: a) Individuen bzw. Paare einer Art wählen als Aufenthalts- oder Brutgebiete nur Land-schaftsformen bzw. Biotope, in denen das artspezifische Ökoschema verwirklicht ist; bei Auswahlmöglichkeit wird dasjenige Habitat bevorzugt, in welchem der Monotop dieser Art relativ am besten ausgeprägt ist. b) Individuen bzw. Paare einer Art können durch intra- bzw. interspezifische Konkurrenz und/oder Interferenz in ihrer Dispersion beeinflußt werden, d. h. durch Rivalität unterlegene Individuen müssen weichen (sofern sie nicht auf das jeweilige Requisit verzichten). c) Dismigrationen von Individuen führen zu Änderungen der popularen Dispersion; diese aktiven Ortsbewegungen sind in ihrem quantitativen und qualitativen Ausmaß artspezifisch. Individuen bzw. Paare einer Art wählen als Aufenthalts- oder Brutgebiete nur Land-schaftsformen bzw. Biotope, in denen das artspezifische Ökoschema verwirklicht ist; bei Auswahlmöglichkeit wird dasjenige Habitat bevorzugt, in welchem der Monotop dieser Art relativ am besten ausgeprägt ist. Individuen bzw. Paare einer Art können durch intra- bzw. interspezifische Konkurrenz und/oder Interferenz in ihrer Dispersion beeinflußt werden, d. h. durch Rivalität unterlegene Individuen müssen weichen (sofern sie nicht auf das jeweilige Requisit verzichten). Dismigrationen von Individuen führen zu Änderungen der popularen Dispersion; diese aktiven Ortsbewegungen sind in ihrem quantitativen und qualitativen Ausmaß artspezifisch. Die Betrachtungen über die Komplexwirkung der drei genannten Faktoren ließen diese als die wichtigsten Dispersionsfaktoren öko-ethologischer Art erkennen. Anhand von sechs Beispielen aus Untersuchungen an waldbewohnenden Höhlenbrütern im südost-niedersächsischen Raum bei Braunschweig wird der Einfluß von Ökoschema, Rivalität und Dismigration auf die brutzeitliche Dispersion dieser Arten aufgezeigt. From the aut-ecological point of view, the concept “eco-scheme” has been proposed and used for the complex of environment-factors comprising the framework necessary for the existance of a species, and for the overall concept for competition (for a requirement in short supply) and for interference (as direct confrontation) the expression “rivalry” has been proposed and used. “Dismigration” is to be understood as including all active movements which lead to a change in dispersion (as the status of spatial separation between individuals of a population). The mentioned eco-ethological dispersion factors are characterised by the fact that both environmental and behavioural elements interact within them. This paper investigates what influence the eco-ethological factors of eco-scheme, rivalry and dismigration exert on the dispersion of individuals within a population. On the basis of results the three following eco-ethological dispersion principles are drawn up: (a) Individuals or pairs of a species choose as resident or breeding grounds only habitats or biotopes in which the species-specific eco-scheme is realised. Where there is a choice, the habitat in which the monotop of this species has been most adequately achieved is preferred. (b) Individuals or pairs of a species may be influenced in their dispersion by intra- or inter-specific competition and/or interference i.e. individuals subordinate in rivalry have to give space (unless they do without the requirement in question). (c) Dismigration of individuals operate in a change in the dispersion of population; these active movements are species-specific quantitatively and qualitatively. Individuals or pairs of a species choose as resident or breeding grounds only habitats or biotopes in which the species-specific eco-scheme is realised. Where there is a choice, the habitat in which the monotop of this species has been most adequately achieved is preferred. Individuals or pairs of a species may be influenced in their dispersion by intra- or inter-specific competition and/or interference i.e. individuals subordinate in rivalry have to give space (unless they do without the requirement in question). Dismigration of individuals operate in a change in the dispersion of population; these active movements are species-specific quantitatively and qualitatively. Studies of the complex effect of the three stated factors indicated these as the most important eco-ethological factors in dispersion. With the help of six examples from studies of woodland hole-breeders in an area of south-east Lower Saxony near Braunschweig, the influence of eco-scheme, rivalry and dismigration on the breeding season dispersion of these species is demonstrated (Fig. 1–6).

Blood sampling does not affect fledging success and fledgling local recruitment in coal tits (Parus ater)

The benefits of extrapair mating behaviour for females of socially monogamous bird species are unclear despite substantial research effort. The genetic compatibility hypothesis proposes genetic benefits such that females paired to social mates of low genetic compatibility avoid or diminish negative fitness consequences by mating with a more compatible extrapair mate, resulting in offspring of higher genetic quality. Furthermore, within the context of inbreeding depression observed in natural populations, a high degree of overall genetic similarity between social pair mates may be regarded as a special case of genetic incompatibility. We tested the hypothesis that female extrapair matings represent an adaptive behavioural response to avoid negative consequences of being paired to a genetically similar social pair male in the coal tit, Parus ater, a socially monogamous passerine with high rates of extrapair paternity. In contrast to what was predicted, we found no evidence for a positive association between the genetic similarity of social pair mates (measured as band-sharing coefficients from multilocus DNA fingerprints) and the occurrence of extrapair paternity. Furthermore, the genetic similarity of the cuckolding female with its social mate was not higher when compared pairwise to that of its extrapair mate in 63 uniquely composed triplets. Finally, three parameters of reproductive success were not related to the genetic similarity of social pair mates. We conclude that avoiding the potentially negative fitness consequences of being paired to a genetically similar social pair mate did not select for and thus cannot maintain female extrapair mating behaviour in our study population. (c) 2004 The Association for tire Study of Animal Behaviour Published by Elsevier Ltd. All rights reserved.