Tim Schmoll

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.

Staying tuned: grasshoppers from noisy roadside habitats produce courtship signals with elevated frequency components

Summary 1. Anthropogenic noise is known to affect acoustic signal production in birds, frogs and mammals. These animals use different mechanisms to adjust their signals to elevated background noise levels (increase in signal amplitude, shift to higher frequencies, etc.). Previous studies have concentrated on behaviourally plastic changes in signal production as a result of elevated background noise levels. To our knowledge, long-term effects of anthropogenic noise on signal production have not yet been investigated. Moreover, strategies of invertebrate species to ensure acoustic signal transmission under anthropogenic noise have not been examined, so far. 2. We tested whether and how male Chorthippus biguttulus grasshoppers from noisy roadside habitats may adjust acoustic courtship signals to elevated background noise levels, compared with conspecifics from quiet control habitats. In this species, sexually selected male courtship signals serve to attract potential mating partners, which make the undisturbed transmission of signals in habitats with increased background noise levels crucial for male reproductive success. 3. Compared to males from control populations, males from roadside habitats produced songs with a significantly higher local frequency maximum under standardized, quiet recording conditions. This local frequency maximum (in the range of c .6 –9 kHz) overlaps with low-frequent road noise that has the potential to degrade or mask this part of the signals’ frequency spectrum. 4. To our knowledge, this is the first evidence that insects from noisy habitats produce different acoustic signals than conspecifics from quiet habitats, possibly using a more permanent mechanism for signal adjustment than behavioural plasticity, which was found in different bird species adjusting to high background noise levels. Such an effect of anthropogenic noise has not been shown for any invertebrate species before, and our results suggest that similar strategies to avoid degradation or masking by noise (i.e. increase in carrier frequency) are used over a wide range of taxa, including both, vertebrates and invertebrates.

Long-term fitness consequences of female extra-pair matings in a socially monogamous passerine.

Whether female birds choose extra–pair mating partners to obtain genetic fitness benefits is intensely debated. The most straightforward and crucial test of ‘good genes’ models of female extra–pair mating is the comparison of naturally ‘cross–fostered’ maternal half–siblings sharing the same rearing environment as any systematic differences in performance between the two categories of offspring phenotype can be attributed to differential paternal genetic contribution. We analysed local recruitment and first–year reproductive performance of maternal half–siblings in the coal tit (Parus ater), a passerine bird with high levels of extra–pair paternity. We provide a highly comprehensive measure of the long–term fitness consequences of female extra–pair matings based on a large sample of 736 within–pair offspring (WPO) and 368 extra–pair offspring (EPO) from 91 first and 55 second broods, from which 132 breeders recruited into the study population. In contrast to predictions derived from ‘good genesrsquo; models, we found no differences in local recruitment and seven parameters of first–year reproductive performance when comparing WPO and EPO. These results question the universal validity of findings in other bird species supporting ‘good genes’ models, particularly as they are based on the best approximation to female fitness obtained so far.

Lifespan, lifetime reproductive performance and paternity loss of within-pair and extra-pair offspring in the coal tit Periparus ater

The hypothesis that females of socially monogamous species obtain indirect benefits (good or compatible genes) from extra-pair mating behaviour has received enormous attention but much less generally accepted support. Here we ask whether selection for adult survival and fecundity or sexual selection contribute to indirect selection of the extra-pair mating behaviour in socially monogamous coal tits (Periparus ater). We tracked locally recruited individuals with known paternity status through their lives predicting that the extra-pair offspring (EPO) would outperform the within-pair offspring (WPO). No differences between the WPO and EPO recruits were detected in lifespan or age of first reproduction. However, the male WPO had a higher lifetime number of broods and higher lifetime number of social offspring compared with male EPO recruits, while no such differences were evident for female recruits. Male EPO recruits did not compensate for their lower social reproductive success by higher fertilization success within their social pair bonds. Thus, our results do not support the idea that enhanced adult survival, fecundity or within-pair fertilization success are manifestations of the genetic benefits of extra-pair matings. But we emphasize that a crucial fitness component, the extra-pair fertilization success of male recruits, has yet to be taken into account to fully appreciate the fitness consequences of extra-pair matings.

How grasshoppers respond to road noise: developmental plasticity and population differentiation in acoustic signalling

Summary Increasing levels of anthropogenic noise have the potential to mask signals of acoustically communicating species in their natural habitats. Animals in noise-polluted habitats typically adjust their signals away from high background noise levels to ensure successful signal transmission under challenging environmental conditions. Earlier we demonstrated that male Chorthippus biguttulus grasshoppers from roadside habitats produce courtship signals with elevated frequency components compared to conspecifics from non-roadside habitats. Here, we use a common garden approach to study the mechanisms underlying this response. We transferred grasshopper nymphs from seven roadside as well as five non-roadside habitats to the laboratory to rear half of them under noisy and the other half under quiet conditions in a full factorial two-by-two design. Courtship songs of adult males were later recorded under standardized quiet conditions. Males exposed to road noise as nymphs produced signals with higher frequency components compared to males reared under quiet conditions, indicating developmental plasticity as a mechanism underlying the signal adjustment to anthropogenic noise in grasshoppers. In addition, males originating from roadside habitats produced signals with higher frequency components and an increased syllable to pause ratio – a sexually selected signal trait – compared to males from non-roadside habitats. Our results demonstrate for the first time that developmental plasticity may play an important role in song trait modifications in response to anthropogenic noise. Furthermore, they suggest that multiple roadside populations may have diverged in parallel, possibly in response to selection for minimizing signal masking by road noise.

Extra-pair paternity, offspring mortality and offspring sex ratio in the socially monogamous coal tit (Parus ater)

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.

A review and perspective on context-dependent genetic effects of extra-pair mating in birds

The evolutionary origin and the maintenance of extra-pair mating in birds has been a major field of study in the last decades, but no consensus has been reached on the adaptive significance of this behaviour for female birds. The genetic benefit hypothesis proposes that extra-pair sires provide alleles of superior quality and/or better compatibility compared to the social mate, resulting in offspring of higher reproductive value. One frequently adopted approach to test this idea compares the performance of maternal half-siblings in broods with multiple paternity. However, results from such comparisons are inconsistent. Here I discuss the concept that the magnitude of genetic fitness benefits from extra-pair mating depends on the environmental context. To date, context-dependent genetic effects in maternal half-sibling comparisons have been demonstrated for only five passerine bird species. In none of the studies were the crucial environmental conditions experimentally manipulated, and the potentially confounding effects of differential maternal investment in relation to paternity were also largely not accounted for. A number of high-quality data sets on fitness consequences of extra-pair mating behaviour are available that could be (re-) analysed for context-dependence given that relevant gradients of the environment have been recorded and their use is well justified a priori. Such relevant variation may include, for example, the time of breeding in temperate regions, hatching order, but also offspring sex. Primarily, however, experimental approaches are required that systematically and gradually vary fitness-relevant environmental gradients, such as food availability or parasite abundance, and analyse the resulting differential fitness effects while controlling for differential investment. The context dependency of the genetic effects of extra-pair mating behaviour may offer an opportunity for reconciling conflicting results from different extra-pair paternity studies within and across species. More generally, it could allow a better understanding of under which environmental conditions will selection act to maintain a female mating bias towards extra-pair males with potentially far-reaching implications for the ecology and evolution of mating preferences and the maintenance of genetic variation in (sexually) selected traits.ZusammenfassungDer evolutionäre Ursprung und die Aufrechterhaltung von außerpaarlichem Kopulationsverhalten bei Vögeln sind in den letzten Jahrzehnten intensiv untersucht worden. Allerdings konnte bisher kein Konsens bezüglich des adaptiven Nutzens dieses Verhaltens für Vogelweibchen erzielt werden. Die genetische Vorteile-Hypothese postuliert, dass Fremdkopulationspartner Genvarianten von höherer Qualität oder besserer Kompatibilität im Vergleich zum sozialen Paarpartner aufweisen, was zu Nachkommen von höherem Reproduktionswert führen würde. Ein häufig genutzter Ansatz zur Überprüfung dieser Hypothese besteht darin, mütterliche Halbgeschwister in Bruten mit multiplen Vaterschaften bezüglich fitness-relevanter Merkmale zu vergleichen. Die Ergebnisse solcher Vergleiche sind allerdings nicht konsistent. In diesem Beitrag diskutiere ich die Idee, dass das Ausmaß genetischer Fitnessvorteile aus Fremdkopulationen vom Umweltkontext abhängt. Kontext-abhängige genetische Effekte wurden bisher nur bei fünf Singvogelarten nachgewiesen. In keiner der betreffenden Studien wurden jedoch die entscheidenden Umweltvariablen experimentell manipuliert. Auch wurden die potentiell konfundierenden Effekte von differentiellem mütterlichen Investment in Abhängigkeit der Vaterschaft zumeist nicht kontrolliert. Eine Reihe von hochqualitativen Datensätzen zu den Fitnesskonsequenzen von Fremdkopulationsverhalten ist verfügbar, die bezüglich ihrer Umweltabhängigkeit (re-) analysiert werden könnten. Dies gilt, sofern relevante Umweltgradienten erfasst wurden und ihre Berücksichtigung a priori plausibel gemacht werden kann. Relevante Variation könnte zum Beispiel den Zeitpunkt des Brütens in gemäßigten Breiten, die Reihenfolge des Schlupfes, aber auch das Geschlecht der Nachkommen umfassen. In erster Linie sind jedoch experimentelle Ansätze nötig, die fitnessrelevante Gradienten der Umwelt wie Futterverfügbarkeit oder Parasitenbelastung systematisch und graduell variieren. Die Kontextabhängigkeit genetischer Effekte von Fremdkopulationen könnte möglicherweise erlauben, widersprüchliche Resultate verschiedener Studien innerhalb und zwischen Arten zu integrieren. Eine solche Kontextabhängigkeit könnte aber auch ganz allgemein helfen zu verstehen, unter welchen Umweltbedingungen Selektion eine weibliche Paarungspräferenz für Fremdkopulationspartner aufrechterhält. Dies hätte potenziell weit reichende Folgen für die Ökologie und Evolution von Paarungspräferenzen und die Aufrechterhaltung genetischer Variation von (sexuell) selektierten Merkmalen.

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

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.

Sperm dimensions differ between two Coal Tit Periparus ater populations

The evolutionary forces that shape and maintain variation in sperm traits across species in birds have recently attracted increased attention. Much less is known about the patterns, the causes and the consequences of variation in sperm traits within and, in particular, between populations of the same species. We here analyse intraspecific variation in sperm dimensions within and between two populations of the Coal Tit Periparus ater, a socially monogamous passerine with a high frequency of extra-pair paternity. Spermatozoa from a Norwegian population had a greater mean total length compared to those from a German population, mainly as a result of longer sperm heads. Sperm head length in the Norwegian population also accounted for a larger percentage of sperm total length suggesting differences in sperm proportions between populations. Furthermore, spermatozoa from the Norwegian population showed lower mean within-male variation in sperm length and there was significant between-male variation in sperm total length within each of the two populations. We discuss these results in the light of recent comparative evidence suggesting relationships between sperm length, and variation in sperm length, and the frequency of extra-pair paternity across passerine birds.ZusammenfassungDie evolutionären Kräfte, die die Variation von Spermienmerkmalen im zwischenartlichen Vergleich geformt und aufrechterhalten haben, erfuhren in jüngerer Zeit gesteigerte Aufmerksamkeit. Viel weniger ist jedoch über die Muster, die Ursachen und die Konsequenzen von innerartlicher Variation von Spermienmerkmalen bekannt, was insbesondere für die Variation zwischen Populationen einer Art gilt. Wir analysieren in diesem Beitrag innerartliche Variation in der Spermienmorphologie der Tannenmeise Periparus ater, einer sozial monogamen Singvogelart mit hohen Fremdvaterschaftsraten. Die Spermatozoen einer norwegischen Population waren im Mittel länger als die einer deutschen Population, was hauptsächlich auf längere Spermienköpfe zurückgeführt werden konnte. Die Spermienköpfe in der norwegischen Population machten auch einen größeren Anteil an der gesamten Spermienlänge aus, was auf Unterschiede in den Spermienproportionen schließen lässt. Darüber hinaus zeigten die Spermatozoen aus der norwegischen Population eine im Mittel niedrigere Variabilität innerhalb eines Ejakulats und die Spermienlänge unterschied sich signifikant zwischen individuellen Männchen in beiden untersuchten Populationen. Wir diskutieren diese Ergebnisse im Lichte aktueller vergleichender Studien, die Zusammenhänge zwischen Spermiengröße bzw. Variation in der Spermiengröße und der Häufigkeit des Auftretens von Fremdvaterschaften nahe legen.

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

In order to assess the potentially harmful consequences of blood sampling in nestling coal tits (Parus ater), we analysed fledging success, fledgling local recruitment and recruit natal dispersal for nestlings originating from 27 blood-sampled broods and nestlings from 39 control broods. No adverse effects of blood sampling were detectable.