性选择、配偶外父亲身份确认程度、遗传变异性和保护

岛屿动物中的性选择强度不高,其原因可能是由于岛屿种群的遗传变异性水平较低。本文作者检验了鸟类岛屿种群是否具有较低的遗传变异性、性选择强度大的种群是否具有较高的突变输入率（rate of mutational input),在鸟类岛屿种群中是否具有较低的性选择强度（可以根据配偶外父亲身份的频率来估计）。小卫星共有谱带系数（minisatellite band sharing coefficient)可确定无亲源关系个体之间的遗传变异性,对与遗传变异性有关的雄性个体的父亲（paternity)进行了成对比较以检验如下假说：在具有较多遗传变异的种群中,雌性个体更经常地进行配偶外交配。在小卫星谱带系数较低的鸟类种群中,配偶外父亲的频次较高。对岛屿和大陆鸟类进行的第二个比较分析表明：岛屿种群中的配偶外父亲频次较低,遗传变异性也较低,其部分原因在于突变输入（mutational input)减少。上述发现表明：（1）父亲确认程度（parternity)随遗传变异性的数量而增加;（2）在遗传变异性较大的种群中,突变率较高,性选择的程度更激烈;（3）岛屿种群中性选择的强度一般比大陆种群弱。这对于理解遗传变异性的空间变异、理解岛屿种群和其它隔离种群的保护问题有重要启示。     

Testosterone, testes size, and mating success in birds: a comparative study

Reproductive behaviors of vertebrates are often underpinned by temporal patterns of hormone secretion. We investigated interspecific patterns of circulating testosterone in male birds to test the hypothesis that testosterone plays a crucial role in sexual selection as determined by degree of polygyny and extra-pair paternity. We predicted that the evolution of increased levels of polygyny and extra-pair paternity would have resulted in the evolution of increased levels of testosterone to allow males more efficiently to compete for mates. This hypothesis was tested in comparative analyses of 116 species of birds using Generalized Least Squares Models. We assessed the importance of latitudinal distribution, because this can confound the relationship between testosterone and mating success. There were weak positive phylogenetic correlations between measures of testosterone and estimates of mating success at the social level, but this association appeared to be confounded by latitudinal distribution, a significant correlate of testosterone titers. However, we found a significantly positive relationship between peak and residual peak testosterone (which is the peak testosterone level that is controlled for the baseline level) and extra-pair paternity independent of latitude. These results suggest that selection pressures arising from social and sexual mating differently affected testosterone levels with the former being mediated by factors associated with latitudinal distribution. An analysis of residual testes size revealed a positive association between peak and residual testosterone and testes size relative to body size. In a path analysis, we show that relative testis size primarily evolved in association with intense sperm competition and thus high sperm production, and these mechanisms had a secondary impact on blood testosterone levels at a phylogenetic scale. Our results suggest that sperm competition has played an important role in the evolution of reproductive mechanisms in birds.     

Extra-pair paternity in birds: explaining variation between species and populations

Molecular techniques used to assign paternity have revealed previously unknown incidences of extra-pair paternity in socially monogamous bird species. DNA fingerprinting has now been used sufficiently often for mating-system biologists to appreciate the natural variation in the frequency of broods showing extra-pair young. The variation between species and between populations of the same species is surprisingly marked. Explaining this variation may help us to understand the factors promoting sexual selection. Recent comparative studies and detailed behavioural studies suggest that factors such as breeding density, genetic variation in the population and the intensity of sexual conflicts determine the costs and benefits to males and females of engaging in extra-pair copulations, and therefore contribute to the variation among populations.     

Immune defence,extra-pair paternity,and sexual selection in birds

Secondary sexual characters have been suggested to reliably reflect the ability of individuals to resist debilitating parasites, and females may gain direct or indirect fitness benefits from preferring the most extravagantly ornamented males. Extra-pair paternity provides an estimate of an important component of sexual selection in birds. Species with a high frequency of extra-pair paternity have a variance in realized reproductive success that is greater than the variance in apparent reproductive success, and extra-pair copulations and hence extra-pair paternity by females are often directly associated with the expression of male secondary sexual characters. If sexually dichromatic species have experienced a long period of antagonistic coevolution with their parasites, such species should have evolved larger immune defence organs than sexually monochromatic species. Bird species with sexual dichromatism had larger spleens for their body size than monochromatic species in a comparative analysis. Furthermore, species with a high frequency of extra-pair paternity were sexually dichromatic and had large spleens for their body size. These results are consistent with the hypothesis that females of dichromatic bird species seek extra-pair copulations to obtain indirect fitness benefits in terms of superior resistance of their offspring to virulent parasites.     

Massive nest-box supplementation boosts fecundity, survival and even immigration without altering mating and reproductive behaviour in a rapidly recovered bird population

Habitat restoration measures may result in artificially high breeding density, for instance when nest-boxes saturate the environment, which can negatively impact species' demography. Potential risks include changes in mating and reproductive behaviour such as increased extra-pair paternity, conspecific brood parasitism, and polygyny. Under particular cicumstances, these mechanisms may disrupt reproduction, with populations dragged into an extinction vortex. With the use of nuclear microsatellite markers, we investigated the occurrence of these potentially negative effects in a recovered population of a rare secondary cavity-nesting farmland bird of Central Europe, the hoopoe (Upupa epops). High intensity farming in the study area has resulted in a total eradication of cavity trees, depriving hoopoes from breeding sites. An intensive nest-box campaign rectified this problem, resulting in a spectacular population recovery within a few years only. There was some concern, however, that the new, high artificially-induced breeding density might alter hoopoe mating and reproductive behaviour. As the species underwent a serious demographic bottleneck in the 1970-1990s, we also used the microsatellite markers to reconstitute the demo-genetic history of the population, looking in particular for signs of genetic erosion. We found i) a low occurrence of extra-pair paternity, polygyny and conspecific brood parasitism, ii) a high level of neutral genetic diversity (mean number of alleles and expected heterozygosity per locus: 13.8 and 83%, respectively) and, iii) evidence for genetic connectivity through recent immigration of individuals from well differentiated populations. The recent increase in breeding density did thus not induce so far any noticeable detrimental changes in mating and reproductive behaviour. The demographic bottleneck undergone by the population in the 1970s-1990s was furthermore not accompanied by any significant drop in neutral genetic diversity. Finally, genetic data converged with a concomitant demographic study to evidence that immigration strongly contributed to local population recovery.     

Extra-pair paternity and song characteristics in the willow warbler Phylloscopus trochilus

Complexity in bird song is often argued to be advantageous in processes of sexual selection, and numerous studies show that characteristics of song are associated with increased success in territory defence or mate attraction. Less evidence exists on the relationship between bird song characteristics and patterns of extra-pair paternity. We tested whether males that suffered from extra-pair paternity differed in song characteristics from males with no extra pair paternity in the willow warbler Phylloscopus trochilus . In the Scottish population that we studied, we found that 23.5% of young were not related to the social father, and that 47% of nests contained at least one extra pair young. Older males were less likely to suffer paternity loss. While song repertoire size was not related to loss of paternity, males with short songs suffered higher paternity loss than males with long songs. Although arrival date is a good correlate of social mate choice in this population, it was not related to extra-pair paternity. These results suggest that females use song length, or a trait correlated with this song characteristic, as a cue for choosing extra-pair partners in this species, or alternatively that variance in the success of mate guarding or female coercion is related to this song variable.     

Extra-pair paternity in the socially monogamous mountain bluebird Sialia currucoides and its effect on the potential for sexual selection

Sexual selection theory posits that ornamental traits can evolve if they provide individuals with an advantage in securing multiple mates. That male ornamentation occurs in many bird species in which males pair with a single female is therefore puzzling. It has been proposed that extra-pair mating can substantially increase the variance in reproductive success among males in monogamous species, thus increasing the potential for sexual selection. We documented the frequency of extra-pair paternity and examined its effect on variation in male reproductive success in the mountain bluebird Sialia currucoides , a socially monogamous songbird in which males possess brilliant plumage ornamentation. Extra-pair paternity was common in our Wyoming study population, with 72% of broods containing at least one extra-pair offspring. The standardized variance in actual male reproductive success (i.e., the total number of within-pair and extra-pair offspring sired) was more than seven times higher than the variation in apparent success (i.e., success assuming that no extra-pair mating occurred). Success at siring within-pair and extra-pair offspring both contributed to the variation in overall male reproductive success. Within-pair success, however, did not predict a male's level of extra-pair success, suggesting that males do not sacrifice within-pair paternity to gain extra-pair paternity. Calculation of the sexual selection (Bateman) gradient showed that males sire approximately two additional offspring for each extra-pair mate that we identified. Thus, in this sexually dichromatic species, extra-pair mating increases the variance in male reproductive success and provides the potential for sexual selection to act.     

Paternity analysis reveals opposing selection pressures on crown coloration in the blue tit (Parus caeruleus)

In socially monogamous species, extra-pair paternity can increase the variance in reproductive success and thereby the potential for sexual selection on male ornaments. We studied whether male secondary sexual ornaments are selected through within- and/or extra-pair reproductive success in the blue tit (Parus caeruleus). Male blue tits display a bright blue crown plumage, which reflects substantially in the ultraviolet (UV) and previously has been indicated to be an important sexual signal. We show that males with a more UV-shifted crown hue were less cuckolded, which probably resulted from female preference for more ornamented mates. By contrast, however, older males and males with a less UV-shifted hue sired more extra-pair young. This probably did not reflect direct female preference, since cuckolders were not less UV-ornamented than the males they cuckolded. Alternatively, a trade-off between UV ornamentation and other traits that enhance extra-pair success could explain this pattern. Our results might reflect two alternative male mating tactics, where more UV-ornamented males maximize within-pair success and less UV-ornamented males maximize extra-pair success. Since crown colour was selected in opposite directions by within-pair and extra-pair paternity, directional selection through extra-pair matings seemed weak, at least in this population and breeding season. Reduced intensity of sexual selection due to alternative mating tactics constitutes a potential mechanism maintaining additive genetic variance of male ornaments.     

Extra-pair paternity in the Skylark Alauda arvensis

We present the first quantitative data on the genetic breeding system of a lark (Alaudidae), the Skylark Alauda arvensis . Using a set of eight microsatellite loci isolated in a variety of passerine species, we genotyped 171 offspring from 52 broods of Skylark and detected 35 extra-pair offspring (20%), in 14 different broods (27%). All offspring matched their putative mother, so there was no evidence of intraspecific brood parasitism. Previous non-genetic studies had suggested that the species was predominantly socially monogamous, with only rare occurrences of social polygyny and polyandry, although some behaviours, such as mate guarding, did suggest the possibility of extra-pair copulations. The relatively high level of extra-pair paternity in this species is likely to affect the variation in male reproductive success because extra-pair paternity was non-randomly distributed amongst males, with those with shorter wings more likely to be cuckolded.     

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 genes' 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.     

Do male paternity guards ensure female fidelity in a duetting fairy-wren?

Most socially monogamous bird species engage in extra-pair mating,and consequently males may adopt various behavioral strategiesto guard paternity. However, the relationship between mate guardingand extra-pair paternity is unclear: low levels of extra-pairpaternity can be associated either with no mate guarding orwith intense mate guarding. We investigate paternity guardsin the purple-crowned fairy-wren (Malurus coronatus), a duettingspecies where extra-pair paternity is rare. This species isunusual in a genus known for extremely high levels of extra-pairmating. We examine the behavioral interactions between the sexesunderlying these low rates of extra-pair paternity and showthat male purple-crowned fairy-wrens do not use frequent copulationor courtship feeding to assure paternity or guard females acousticallyby duetting. Males maintain close proximity to females bothwhen they are fertile and when they are not breeding and donot invest in courtship displays to extra-pair females. Consistentwith predictions of theoretical models, low extra-pair paternityin this species may be related to female fidelity rather thanmale paternity assurance strategies, but short-term removalof males would be necessary to test this experimentally.     

Captive breeding and reintroduction of the lesser kestrel Falco naumanni: a genetic analysis using microsatellites

We used microsatellites to assess ongoing captive breeding and reintroduction programs of the lesser kestrel. The extent of genetic variation within the captive populations analysed did not differ significantly from that reported in wild populations. Thus, the application of widely recommended management practices, such as the registration of crosses between individuals in proper stud books and the introduction of new individuals into the genetic pools, has proven satisfactory to maintain high levels of genetic variation. The high rates of hatching failure occasionally documented in captivity can therefore not be attributed to depressed genetic variation. Even though genetic diversity in reintroduced populations did not differ significantly when compared to wild populations either, average observed heterozygosities and inbreeding coefficients were significantly lower and higher, respectively, when compared to the captive demes where released birds came. Monitoring of reproductive parameters during single-pairing breeding and paternity inference within colonial facilities revealed large variations in breeding success between reproductive adults. The relative number of breeding pairs that contributed to a large part of captive-born birds (50–56%) was similar in both cases (28.6 and 26.9%, respectively). Thus, the chances for polygyny (rarely in this study), extra-pair paternity (not found in this study) and/or social stimulation of breeding parameters do not seem to greatly affect the genetically effective population size. Independently of breeding strategies, the release of unrelated fledglings into the same area and the promotion of immigration should be mandatory to counteract founder effects and avoid inbreeding in reintroduced populations of lesser kestrels.     

Extra-pair paternity does not result in differential sexual selection in the mutually ornamented black swan (Cygnus atratus)

We studied patterns of parentage in 85 broods (332 cygnets) of black swans during three breeding seasons, using a set of eight polymorphic microsatellite markers. We detected both intraspecific brood parasitism (IBP; < 5% of cygnets per year) and extra-pair paternity (EPP). In these years, 10-17% (mean = 15.1%) of cygnets resulted from EPP, and 27-40% (mean 37.6%) of broods contained at least one extra-pair cygnet. Compared with levels of EPP in closely related species with similar life histories, these values are unexpectedly high. EPP in black swans appears unrelated to ecological factors (breeding density and synchrony) or genetic factors (genetic similarity between pair members or genetic quality of the offspring). We found no evidence that a mutual sexual feather ornament known to play a role in social mate choice in black swans (curled wing feathers) is involved in extra-pair mate choice. EPP does not lead to greater variance in reproductive success in males, relative to females in this species. We therefore suggest that EPP does not result in differential sexual selection on males and females, explaining why they are ornamented to the same degree.     

Rock sparrow song reflects male age and reproductive success

The evolution of mating signals is closely linked to sexual selection. Acoustic ornaments are often used as secondary sexual traits that signal the quality of the signaller. Here we show that song performance reflects age and reproductive success in the rock sparrow (Petronia petronia). In an Alpine population in south-east France, we recorded the songs of males and assessed their genetic breeding success by microsatellite analysis. In addition to temporal and spectral song features, we also analysed for the first time whether the sound pressure level of bird song reflects reproductive success. Males with higher breeding success sang at a lower rate and with a higher maximum frequency. We found also that older males gained more extra-pair young and had a higher overall breeding success, although they also differed almost significantly by having a higher loss of paternity in their own nests. Older males could be distinguished from yearlings by singing at lower rate and higher amplitudes. Our findings suggest that song rate may be used as a signal of age and together with song pitch as a signal of reproductive success in this species. Alternatively, younger and less successful males might try to compensate their inferior status by increased song rates and lower pitch. Independent of age and quality, high-amplitude songs correlated with paternity loss in the own nest, suggesting that in this species song amplitude is not an indicator of male quality but high-intensity songs may be rather a response to unfaithful social mates.     

The distribution of extra-pair young within and among broods – a technique to calculate deviations from randomness

Molecular paternity tests show that extra-pair fertilizations are common in many socially monogamous bird species. However, the question of why females often seek extra-pair copulations is still controversial. Competing alternative explanations differ in their predictions on how extra-pair young should be distributed within and among broods. Analysing these distributions may therefore help to resolve this controversy. In several species broods without extra-pair young and those with total or nearly total extra-pair paternity have been claimed to be over-represented. Consequently, extra-pair nestlings would be distributed non-randomly among nests. To compute expected frequencies (i.e. the patterns of random distribution) the Poisson distribution has frequently been used. However, the Poisson distribution is not appropriate for two reasons. (1) Impossible configurations can receive positive probabilities. (2) The Poisson distribution approaches randomness only if extra-pair fertilizations are events of low probability, which often is not the case. We show how randomness can be computed appropriately by using the multivariate hypergeometric distribution. Re-analysing published data on distributions of extra-pair young, we show that the result that there are more broods containing either none or many extra-pair young than expected by chance is even more pronounced than previously thought.     

Multiple ornamentation, female breeding synchrony, and extra-pair mating success of golden whistlers (Pachycephala pectoralis)

Considerable variation exists in rates of extra-pair paternity between species, and across and within populations of the same species. Explanations for this variation include ecological (e.g. breeding synchrony), morphological (e.g. ornamentation), and genetic (e.g. relatedness) factors, but it is rare for studies to simultaneously explore these factors within a single population. This is especially true for highly ornamented species, where mate choice based on ornamentation may be more complex than in less-adorned species. We conducted such a study in a migratory population of the highly ornamented golden whistler (Pachycephala pectoralis). We quantified male genetic reproductive success and related it to a range of factors putatively involved in determining extra-pair mating success. We found no effects of genetic factors (male heterozygosity and relatedness) on extra-pair success, nor of territory size, male age, or incubation effort. Instead, males possessing yellower breast plumage and large song repertoires enjoyed higher reproductive success. Additionally, we found a negative relationship between local breeding synchrony and male extra-pair mating success. This may be a consequence of mate guarding during the female fertile period and an inability of males to simultaneously mate-guard and pursue extra-pair fertilisations. In this species, the opportunity for extra-pair matings appears to vary temporally with an ecological variable (local breeding synchrony), while fine-scale, inter-male differences in mating success may be influenced by individual attributes (male ornamentation). The migratory nature of the study population and its lack of natal philopatry may mean that relatedness and inbreeding avoidance are less important considerations in mate choice.     

Sexual size dimorphism and sexual selection in primates

1. In most animals, females are larger than males. Paradoxically, sexual size dimorphism is biased towards males in most mammalian species. An accepted explanation is that sexual dimorphism in mammals evolved by intramale sexual selection. I tested this hypothesis in primates, by relating sexual size dimorphism to seven proxies of sexual selection intensity: operational sex ratio, mating system, intermale competition, group sex ratio, group size, maximum mating percentage (percentage of observed copulations involving the most successful male), and total paternity (a genetic estimate of the percentage of young sired by the most successful male).
2. I fitted phylogenetic generalised least squares models using sexual size dimorphism as the dependent variable and each of the seven measures of intensity of sexual selection as independent variables. I conducted this comparative analysis with data from 50 extant species of primates, including Homo sapiens, Pan troglodytes, and Gorilla spp.
3. Sexual dimorphism was positively related to the four measures of female monopolisation (operational sex ratio, mating system, intermale competition, and group sex ratio) and in some cases to group size, but was not associated with maximum mating percentage or total paternity. Additional regression analyses indicated that maximum mating percentage and total paternity were negatively associated with group size.
4. These results are predicted by reproductive skew theory: in large groups, males can lose control of the sexual behaviour of the other members of the group or can concede reproductive opportunities to others. The results are also consistent with the evolution of sexual size dimorphism before polygyny, due to the effects of natural, rather than sexual, selection. In birds, the study of molecular paternity showed that variance in male reproductive success is much higher than expected by behaviour. In mammals, recent studies have begun to show the opposite trend, i.e. that intensity of sexual selection is lower than expected by polygyny.
5. Results of this comparative analysis of sexual size dimorphism and sexual selection intensity in primates suggest that the use of intramale sexual selection theory to explain the evolution of polygyny and sexual dimorphism in mammals should be reviewed, and that natural selection should be considered alongside sexual selection as an evolutionary driver of sexual size dimorphism and polygyny in mammals.

     

Trade up polygyny and breeding synchrony in avian populations

The advent of the molecular techniques used to assign paternity has focused attention on the differences between the social and the genetic mating systems of sexual species. In particular, the interrelations between breeding synchrony-the degree to which the fertility periods of individual females in a population overlap and the degree of extra pair paternity (EPP) in that population, has became a subject of a lively debate. Investigation of the subject can be facilitated by examining the criteria that females use in choosing extra pair partners. These preferences constitute a continuum ranging between two extremes. At one end, there are situations wherein all the females in a population exhibit a preference for males with particular phenotypic markers, and females mated to males lacking such "quality" markers seek extra pair fertilizations from males that do -trade up polygyny. At the other extreme, there are situations wherein females seek to maximize the total number of male partners, rather than secure fertilization by males of particular type -indiscriminate polygyny. Previously, we used game theoretical methods to model the interrelations between breeding synchrony and EPP in the context of indiscriminate polygyny. Here we present an analogous investigation in the context of trade up polygyny. Our results for the two cases, which delimit the range of the possible behavior, are similar. That is, we see that it is the pursuit of extra pair fertilizations opportunities that determines breeding synchrony of populations, rather than the vice versa as has been previously suggested.     

Long-term paternity skew and the opportunity for selection in a mammal with reversed sexual size dimorphism

Most mammalian groups are characterized by male-biased sexual size dimorphism, in which size-dependent male-male competition and reproductive skew are tightly linked. By comparison, little is known about the opportunity for sexual selection in mammalian systems without male-biased dimorphism, where the traits under sexual selection might be less obvious. We examined 10 years of parentage data in a colony of greater horseshoe bats (Rhinolophus ferrumequinum) to determine the magnitude of male reproductive skew and the opportunity for sexual selection in a mammal in which females are the larger sex. Annual paternity success was weakly skewed but consistent patterns led to strong longitudinal paternity skew among breeders. Just three males accounted for a third of all paternity assignments, representing at least a fifth of all colony offspring born in a decade. Paternity success was in part determined by age but was not influenced by dispersal status. Our results show that paternity skew and the opportunity for sexual selection in a species with reversed sexual size dimorphism can approach levels reported for classical examples of species with polygyny and male-biased dimorphism, even where the traits under sexual selection are not known.     

Sperm competition and sexually size dimorphic brains in birds

Natural selection may favour sexually similar brain size owing to similar selection pressures in males and females, while sexual selection may lead to sexually dimorphic brains. For example, sperm competition involves clear-cut sex differences in behaviour, as males display, mate guard and copulate with females, while females choose among males, and solicit or reject copulations. These behaviours may require fundamentally different neural government in the two sexes leading to sex-dependent brain evolution. Using two phylogenetic approaches in a comparative study, we tested for roles of both natural and sexual-selection pressures on brain size evolution of birds. In accordance with the natural-selection theory, relative brain size of males coevolved with that of females, which may be the result of adaptation to similar environmental constraints such as feeding innovation. However, the mode of brain size evolution differed between the sexes, and factors associated with sperm competition as reflected by extra-pair paternity may give rise to sexually size dimorphic brains. Specifically, species in which females have larger brains than males were found to have a higher degree of extra-pair paternity independently of potentially confounding factors, whereas species in which males have relatively larger brains than females appeared to have lower rates of extra-pair paternity. Hence, the evolution of sperm competition may select for complex behaviours together with the associated neural substrates in the sex that has a higher potential to control extra-pair copulations at the observed levels. Brain function may thus be affected differently in males and females by sexual selection.