Consequences of being unfaithful : costs and benefits of extra pair copulations in birds

Die bedeutendste Entdeckung der letzten 30 Jahre in Bezug auf das Fortpflanzungsverhalten von Vögeln war die Erkenntnis, dass es bei mehr als 80% aller sozial monogamen Singvogelarten regelmäßig zu Kopulationen außerhalb des Paarbundes kommt („extra-pair copulations“; EPCs). In der Folge setzte sich eine beeindruckende Zahl von Untersuchungen mit verschiedenen Aspekten dieses Verhaltens auseinander. Neben Studien, die sich mit Unterschieden in der Häufigkeit des Auftretens von „Fremdvaterschaften” bei verschiedenen Vogelarten beschäftigten, wurden vor allem Untersuchungen zum Kosten und Nutzen von EPCs für Männchen und Weibchen durchgeführt. Auf der Basis eigener Untersuchungen, die dazu dienten, das genetische Paarungssystem von sozial monogamen Kohl- und Tannenmeisen (Parus major and P. ater) zu ergründen, werden hier einige Resultate dieser Bemühungen und auch die ihnen zugrundeliegenden Überlegungen dargestellt. Kosten von EPCs beinhalten für Weibchen möglicherweise eine Reduktion in der Brutfürsorge durch die Männchen, weil die Anzahl eigener Nachkommen und damit der Fortpflanzungswert einer Brut für „betrogene“ Männchen abnimmt. In Übereinstimmung mit dieser Hypothese fanden wir, dass sich die Brutverteidigung männlicher Kohlmeisen nach der Anzahl eigener Nachkommen und nicht nach der Brutgröße richtet. Außerdem fütterten „betrogene“ Männchen ihre Bruten weniger als nicht „betrogene“ Männchen. Wenn EPCs den Weibchen Kosten verursachen, so muss auf der anderen Seite ein entsprechender Nutzen vorhanden sein, da Selektion sonst zum Verschwinden dieses Verhaltens führen sollte. Während männliche Kohl- und Tannenmeisen ihren Fortpflanzungserfolg durch EPCs direkt erhöhen können, ist ein Nutzen für die Weibchen nicht derart offensichtlich. Bei der Analyse einer großen Zahl von Tannenmeisenbruten konnten wir keinerlei Hinweis dafür finden, dass die vieldiskutierten „Gute Gene”-Modelle den Nutzen von EPCs für Weibchen erklären. Würden Weibchen durch EPCs „bessere“ oder „kompatiblere“ väterliche Gene für die betreffenden Nachkommen erhalten, wäre zu erwarten, dass EPY ihren Halbgeschwistern in irgendeiner Form überlegen sind. Zwischen den beiden Halbgeschwistergruppen fand sich jedoch weder in Bezug auf die Überlebenswahrscheinlichkeit noch in Bezug auf den Fortpflanzungserfolg im ersten Brutjahr ein Unterschied. Aus diesen und anderen Befunden wird geschlossen, dass „Gute Gene”-Modelle das weit verbreitete Auftreten von EPCs bei Vögeln alleine kaum erklären können und dass wahrscheinlich mehr als ein einzelner Selektionsfaktor die Evolution dieses Verhaltens bei Vögeln beeinflusst hat.The most important discovery with respect to avian mating systems in the last three decades was the finding that extra-pair paternity occurs regularly in over 80% of all passerine bird species that were cursorily classified as monogamous in the past. Not surprisingly, this insight entailed an impressive body of research focussing on different aspects of this behavioural pattern. Besides analyses of the variation in the frequency of extra-pair paternity, particularly potential costs and benefits of xtra-pair copulations for (individual) males and females had been analysed. Some results of this effort and the rationales behind it are exemplified here, by detailing own work that was performed to investigate the genetic mating systems of socially monogamous great and coal tits (Parus major and P. ater). Costs of extra-pair copulations for females potentially involve a decrease in paternal care, since the number of own offspring and therefore the reproductive value of a brood decreases for cuckolded males. In agreement with this hypothesis we found, that nest defence of male great tits was related to the number of offspring fathered by themselves, but not to brood size per se. Furthermore, cuckolded males fed their broods less frequently than non-cuckolded males. Since extra-pair matings seem to be costly to females, also some benefits of extra-pair copulations have to be postulated, as otherwise selection should act against its occurrence. While male great and coal tits benefit through extra-pair paternity by directly increasing their reproductive success, the benefits for females are far less clear. By studying a large number of coal tit broods, we were unable to provide evidence that “good genes” models can explain the benefits resulting from extra-pair copulations for females. Neither survival probability nor first year reproductive performance of extra-pair young and their maternal half-siblings differed, indicating that females cannot increase their reproductive success by obtaining “higher quality” or “more compatible” paternal genes through extra-pair matings. Based on these and other results it is argued, that “good genes” models alone can hardly explain the occurrence and maintenance of extra-pair paternity in birds in general and that presumably more than a single selective pressure has shaped the evolution of female multiple mating in birds

Molecular genetic evidence for mixed maternity in broods of the Coal Tit Parus ater

Mittels molekulargenetischer Elternschaftsanalyse wurde eine niedrige Rate gemischter Mutterschaften in Bruten der sozial monogamen Tannenmeise nachgewiesen, einer Art, die sich durch hohe Fremdvaterschaftsraten auszeichnet. Gemischte Mutterschaften wurden in vier (= 0,8 %) von 483 Bruten entdeckt und nur für zehn (= 0,3 %) von 3563 erfolgreich genotypisierten Nachkommen wurde die Putativmutter von der genetischen Mutterschaft ausgeschlossen. In Anbetracht dieser sehr niedrigen Rate kann in evolutionsbiologischen Studien der soziale Fortpflanzungserfolg mit dem genetischen Fortpflanzungserfolg für Weibchen der Tannenmeise ohne weiteres gleichgesetzt werden. Die Putativväter wurden ebenfalls in allen Fällen von der genetischen Elternschaft ausgeschlossen, was Quasiparasitismus als Erklärung für gemischte Mutterschaften ausschließt. In einem Fall konnten die Partner eines Brutpaares, das zeitgleich in der Nähe eine eigene Brut aufzog, zweifelsfrei als die genetischen Eltern eines einzelnen Nachkommen identifiziert werden. Mögliche Ursachen für das Auftreten gemischter Mutterschaften bei der Tannenmeise schließen die Übernahme von Nistkästen samt begonnenen Gelegen nach dem Tod oder Abwandern der Vorbesitzer und innerartlichen Brutparasitismus ein.Molecular genetic analysis of parentage revealed a low frequency of mixed maternity in broods of the Coal Tit, a socially monogamous passerine with a high frequency of extra-pair paternity. Mixed maternity was detected in four (= 0.8 %) out of 483 analysed broods. For ten (= 0.3 %) out of 3563 successfully genotyped offspring the attending putative (social) mother was excluded from genetic parentage. Given the very low frequency of mixed maternity, social reproductive success can conveniently be equated with genetic reproductive success for female Coal Tits in evolutionary studies. Attending putative fathers were excluded from genetic parentage in all cases, too, ruling out quasi-parasitism as a mechanistic explanation for mixed maternity. In one case, the pair members from an adjacent territory were unequivocally identified as the genetic parents of a single offspring (they were simultaneously attending their own brood). Possible mechanisms leading to mixed maternity broods in the Coal Tit may include nest/clutch take-over and intraspecific brood parasitism and their respective relevance is briefly discussed

Ornamental non-carotenoid red feathers of wild burrowing parrots

Bird plumage colors have the potential to indicate individual quality, condition, health, immunocompetence, or the extend of parental care. Color intensity of feathers has been found to correlate with parameters of individual quality, condition, parental care and breeding success. Psittaciformes are well known for their colorful plumage but the significance of parrot coloration is still poorly understood. Red colors are very common in many parrot species. They are produced by at least four non-carotenoid-based pigments (linear polyenal structure). In the present study, we investigated a collection of red abdominal feathers of a marked population of wild Burrowing Parrots Cyanoliseus patagonus in Patagonia, Argentina. The aims of this study were to investigate the ecological significance of the recently described non-carotenoid-based red pigments of Psittaciformes, and the relationships between objectively assessed plumage color and body size, body condition, breeding success and nestling growth in wild Psittaciformes. We found that sexes differed in plumage coloration (sexual dichromatism), that plumage color was a good predictor of female body condition and male size, and we identified the red coloration of the abdominal patch as a signal of individual quality and parental investment.Facultad de Ciencias Naturales y Muse

Yearling male great tits, Parus major, suffer more strongly from cuckoldry than older males

Lubjuhn T, Gerken T, Bruen J, Schmoll T. Yearling male great tits, Parus major, suffer more strongly from cuckoldry than older males. ZOOLOGY. 2007;110(5):387-397.In the majority of socially monogamous bird species, females have offspring sired by males other than their social mate as the result of extra-pair copulations. While it is widely recognised that there is considerable variation in the frequency of extra-pair paternity between species, between populations of a species and between individuals of a population, determinants of this variation are surprisingly difficult to establish. With respect to individual variation within a population, it is an important step to test for male and female correlates of cuckoldry to better understand the patterns as well as the adaptive significance of extra-pair mating behaviour. Here, we analysed patterns of extra-pair paternity in relation to male age, female age and their interaction in the great tit Parus major, a socially monogamous passerine with a moderate frequency of extra-pair paternity. Based on a large sample of 316 genotyped first broods from five successive years, we failed to demonstrate interaction effects of male and female age on both the proportion of extra-pair offspring and the likelihood that at least one extra-pair offspring is present within a brood. However, both the proportion of extra-pair offspring and the likelihood of paternity loss were higher for yearling as compared to older males, while this was not the case for yearling vs. older females. Furthermore, the proportion of extra-pair offspring within a brood decreased with increasing age of the attending male in within-individual analyses. We found a comparable effect also for attending females in within-individual analyses, but only when excluding two individuals with 100% extra-pair paternity. A female (extra-pair) mating preference for older males and/or a limited ability of yearling males to prevent cuckoldry in their broods could explain these age-related patterns of paternity loss. Effect sizes, however, were not particularly large and substantial residual variation within age categories suggests the importance of further yet unidentified determinants of variation in paternity loss in the study population. (C) 2007 Elsevier GmbH. All rights reserved

Truly hypervariable DNA fingerprints due to exceptionally high mutation rates

Lubjuhn T, Sramkova A, Masello J, Quillfeldt P, Epplen JT. Truly hypervariable DNA fingerprints due to exceptionally high mutation rates. ELECTROPHORESIS. 2002;23(4):517-519.The power of DNA fingerprinting is due to comparatively high mutation rates of minisatellite and microsatellite DNA sequences. Studying the mating system of a parrot species (Burrowing Parrots, Cyanoliseus patagonus) using oligonucleotide probes, we observed mutation rates that are several orders of magnitude higher than those described anywhere in the literature. Most plausibly, the respective values are based on 3–4 loci with mutation rates of up to 100%

Ornamental non‐carotenoid red feathers of wild burrowing parrots

Masello J, PAGNOSSIN ML, LUBJUHN T, QUILLFELDT P. Ornamental non‐carotenoid red feathers of wild burrowing parrots. Ecological Research. 2004;19(4):421-432.Bird plumage colors have the potential to indicate individual quality, condition, health, immunocompetence, or the extend of parental care. Color intensity of feathers has been found to correlate with parameters of individual quality, condition, parental care and breeding success. Psittaciformes are well known for their colorful plumage but the significance of parrot coloration is still poorly understood. Red colors are very common in many parrot species. They are produced by at least four non‐carotenoid‐based pigments (linear polyenal structure). In the present study, we investigated a collection of red abdominal feathers of a marked population of wild Burrowing ParrotsCyanoliseus patagonusin Patagonia, Argentina. The aims of this study were to investigate the ecological significance of the recently described non‐carotenoid‐based red pigments of Psittaciformes, and the relationships between objectively assessed plumage color and body size, body condition, breeding success and nestling growth in wild Psittaciformes. We found that sexes differed in plumage coloration (sexual dichromatism), that plumage color was a good predictor of female body condition and male size, and we identified the red coloration of the abdominal patch as a signal of individual quality and parental investment

Genetic monogamy in burrowing parrots ?

Masello J, Sramkova A, Quillfeldt P, Epplen JT, Lubjuhn T. Genetic monogamy in burrowing parrots ? Journal of Avian Biology. 2002;33(1):99-103.We report on a first DNA fingerprinting study of paternity in a Psittaciform bird, the burrowing parrotCyanoliseus patagonus. In two consecutive breeding seasons, a total of 49 families was sampled, of which 11 breeding pairs were investigated each of two years. Extra‐pair paternity was not encountered suggesting that burrowing parrots are socially as well as genetically monogamous. Strict genetic monogamy is comparatively rare in birds and occurs predominantly in some groups of non‐passeriformes all of which exhibit long reproductive lifespans and essential paternal care. Psittaciformes fit this pattern. We conclude that paternal care plays a crucial role in the evolution and maintenance of genetic monogamy in the study species. Cases of intraspecific brood parasitism are rarely observed

Nuptial feeding in the scorpionfly Panorpa vulgaris: Maintenance of genetic variance in sexual advertisement through dependence on condition influeincing traits

Missoweit M, Engqvist L, Lubjuhn T, Sauer KP. Nuptial feeding in the scorpionfly Panorpa vulgaris: Maintenance of genetic variance in sexual advertisement through dependence on condition influeincing traits. Evolutionary Ecology. 2008;22(5):689-699.In Panorpa vulgaris scorpionflies, females choose males on the basis of their saliva secretion ability depending on salivary gland weight. Condition dependent salivary gland weight indicates male quality in terms of food acquisition ability (FAA). In the present study we compare standardised estimates of additive genetic variance (V (a)) in conditional status and salivary gland weight under conditions including and excluding food competition. Estimates of V (a) were high when individuals compete for food and significantly lower when food competition was excluded, indicating that a large proportion of V (a) in conditional status as well as salivary gland weight attributes to V (a) in FAA. As FAA is likely to be determined by various underlying traits, maintenance of V (a) in FAA, and therewith in salivary gland weight, is easily conceivable. Furthermore, we found a strong genetic correlation between condition and salivary gland weight under conditions including food competition that decreased when food competition was excluded and thereby diminished the strength of sexual selection on condition influencing traits. In sum, our results demonstrate that estimates of V (a) in sexual signals (especially if estimated using standardised breeding conditions) will be strongly influenced by the presence/absence of environmental factors related to male performance in natural selection context