Extrapair paternity in the great tit (Parus major): a test of the "good genes" hypothesis

In 1993 and 1994 we determined the frequency of extrapair paternityin broods of great tits, Parus major using multilocus DNA fingerprinting.We found no instances of intraspecific brood parasitism, but40% of broods (31/78) contained extrapair-fathered young and83% of offspring (58/681) were xtrapair We identified the geneticfathers of 60% of the extrapair nestlings (35/ 58). Males withfull and lost paternity did not differ significantly in traitsthat have been suggested to indicate male quality, nor did thegenetic and social fathers of extrapair offspring. In 1993,cuckolded males sired more offspring that recruited to the subsequentbreeding season than males with full paternity. Moreover, eventhough genetic fathers of extrapair young (EPY) sired more fledglingsthan the males they cuckolded, genetic and social fathers ofEPY did not differ in the number of recruits sired. Also, theEPY of a brood did not survive better than their half sibs.Thus, our results do not supportthe hypothesis that femaleschoose better quality males for extrapair matings ("good genes"hypothesis). Further, the level of extrapair paternity differedmarkedly between the two years. Our data show that females areconstrained in their extrapair activities by the availabilityof extrapair mates. This is at least partly due to yearly differencesin breeding synchrony.     

No effect of parental quality or extrapair paternity on brood sex ratio in the blue tit (Parus caeruleus)

Sex allocation theory predicts that parents should manipulatebrood sex ratio in order to maximise the combined reproductivevalue of their progeny. Females mating with high quality malesshould, therefore, be expected to produce brood sex ratiosbiased towards sons, as male offspring would receive a relativelygreater advantage from inheritance of their father's characteristicsthan would their female siblings. Furthermore, it has been suggested that sex allocation in chicks fathered through extrapair fertilizations should also be biased towards sons. Contraryto these predictions, we found no evidence that the distributionof sex ratios in a sample of 1483 chicks from 154 broods ofblue tits (Parus caeruleus) deviated significantly from thatof a binomial distribution around an even sex ratio. In addition,we found no significant effect on brood sex ratio of the individualquality of either parent as indicated by their biometrics, feather mite loads, time of breeding, or parental survival. This suggeststhat females in our population were either unable to manipulateoffspring sex allocation or did not do so because selectionpressures were not strong enough to produce a significant shiftaway from random sex allocation. The paternity of 986 chicks from 103 broods was determined using DNA microsatellite typing.Extrapair males sired 115 chicks (11.7%) from 41 broods (39.8%).There was no significant effect of paternity (within-pair versusextrapair) on the sex of individual offspring. We suggest that,in addition to the weakness of selection pressures, the possiblemechanisms responsible for the allocation of sex may not besufficiently accurate to control offspring sex at the levelof the individual egg.     

Sex ratio and male sexual characters in a population of blue tits, Parus caeruleus

Sex allocation theory proposes that parents should bias thesex ratio of their offspring if the reproductive value of onesex is greater than that of the other. In the monogamous bluetit (Parus caeruleus), males have a greater variance in reproductivesuccess than females, and high-quality males have higher reproductivesuccess than high-quality females due to extrapair paternity.Consequently, females mating with attractive males are expectedto produce broods biased toward sons, as sons benefit more thandaughters from inheriting their father's characteristics. Songand plumage color in birds are secondary sexual characters indicatingmale quality and involved in female choice. We used these malesexual traits in blue tits to investigate adaptive sex ratiomanipulation by females. We did not find any relationship betweenmale color ornamentation and brood sex ratio, contrary to previousstudies. On the other hand, the length of the strophe bout (i.e.,the mean number of strophes per strophe bout) of fathers waspositively related with the proportion of sons in their broods.The length of the strophe bout is supposed to reflect male qualityin terms of neuromuscular performance. We further showed thatsons produced in experimentally enlarged broods had shorterstrophe bouts than sons raised in reduced broods. These resultsare consistent with the hypothesis that females adjust the sexratio of their broods in response to the phenotype of theirmate.     

Ultraviolet reflectance affects male-male interactions in the blue tit (Parus caeruleus ultramarinus)

Several animal species have been shown to use phenotypic traitsto assess the competitive ability of opponents and adjust theiraggressiveness depending on the likelihood to win the contest.In birds, these phenotypic traits usually involve patches ofcolored feathers. The benefit to harbor honest signals of malequality is the avoidance of wasteful aggressive interactions.Recent work has shown that ultraviolet (UV) plumage reflectanceis an important signal used by females during mate choice. Surprisingly,however, the role of UV signaling on intrasexual selection hasbeen neglected. In the present study, we aimed to test whetherUV reflectance of crown feathers was used as a signal of malecompetitive ability during male-male interactions. Breedingmale blue tits (Parus caeruleus ultramarinus) were exposed duringthe female egg-laying period to blue tit taxidermic mounts witheither control or reduced UV reflectance of crown feathers.In agreement with the prediction that UV reflectance advertisesmale quality, we found that breeding blue tits behaved lessaggressively toward the UV-reduced decoy. To our knowledge,this is the first experimental evidence suggesting a role forUV signaling on intrasexual selection.     

Cryptic male choice: sperm allocation strategies when female quality varies

We examined evolutionary stable sperm allocation and included stochastic variation in male mating frequency, not included in previous models examining sperm allocation strategies. We assumed sperm mixing and variation in female quality and used a genetic algorithm to analyse the evolution of male sperm allocation. Our results show that males should invest more sperm in initial copulations than in subsequent copulations as a male might fail to mate again. The inclusion of variation in female fecundity had no influence on the evolutionary stable sperm allocation strategy if males were unable to recognize female quality. If males were assumed to allocate sperm in response to female quality, the proportion of sperm allocated was positively correlated with female quality. Moreover, with increasing variance in female quality, males conserved more sperm for later copulations. Literature data on sperm allocation from diverse taxa show a good fit with the predictions given by our model.     

Extrapair paternity and mate choice in a chickadee hybrid zone

The dynamics of hybrid zones are likely to be influenced greatlyby patterns of mate choice, including "cryptic" choice mediatedthrough extrapair copulations. To understand changes in hybridzones over time and space, a detailed examination of matingpatterns and correlates is needed. We studied the role of extrapairfertilizations (EPFs) in the breeding biology of hybridizingblack-capped and Carolina chickadees in southeastern Pennsylvaniaover 4 years, using microsatellite DNA markers. We detectedextrapair offspring (EPO) in 56% of 90 broods examined; theseaccounted for at least 26% of 477 offspring. Chickadees do notappear to use EPFs to reduce costs of heterospecific pairing:EPFs were no more likely to occur in genetically dissimilar(heterospecific) social pairs than in pairs where social mateswere genetically similar. However, females paired with black-capped–likemales were more likely to have EPO. Females that acquired EPFsdid not obtain these from males genetically similar to themselves;instead, all females, regardless of their genotype or that oftheir social mate, tended to prefer Carolina-like males as extrapairpartners. There was no relationship between the presence ofEPO and hatching or fledging success. High rates of extrapairpaternity and apparent female preference for Carolina-like malessuggest that mate choice is an important influence in ongoingnorthward movement of this hybrid zone.     

Heritability of female extra-pair paternity rate in song sparrows (Melospiza melodia)

The forces driving the evolution of extra-pair reproduction in socially monogamous animals remain widely debated and unresolved. One key hypothesis is that female extra-pair reproduction evolves through indirect genetic benefits, reflecting increased additive genetic value of extra-pair offspring. Such evolution requires that a female's propensity to produce offspring that are sired by an extra-pair male is heritable. However, additive genetic variance and heritability in female extra-pair paternity (EPP) rate have not been quantified, precluding accurate estimation of the force of indirect selection. Sixteen years of comprehensive paternity and pedigree data from socially monogamous but genetically polygynandrous song sparrows (Melospiza melodia) showed significant additive genetic variance and heritability in the proportion of a female's offspring that was sired by an extra-pair male, constituting major components of the genetic architecture required for extra-pair reproduction to evolve through indirect additive genetic benefits. However, estimated heritabilities were moderately small (0.12 and 0.18 on the observed and underlying latent scales, respectively). The force of selection on extra-pair reproduction through indirect additive genetic benefits may consequently be relatively weak. However, the additive genetic variance and non-zero heritability observed in female EPP rate allow for multiple further genetic mechanisms to drive and constrain mating system evolution.     

Repertoire size, sexual selection, and offspring viability in the great reed warbler: changing patterns in space and time

Only a few studies have focussed on the consistency of sexualselection patterns in space and time. One such case is the greatreed warbler (Acrocephalus arundinaceus), for which studiesin Germany in 1981–1982 and Sweden in 1987–1991strongly suggested that the size of a male's song repertoirewas the target of mate choice and sexual selection. Studyingthe same German population once again in 1994–2000, weinvestigated the consistency of these patterns over time aswell as between populations. Our reanalysis of the data from1981–1982 shows that male repertoire size was positivelycorrelated with male pairing success (harem size) and with clutchsize (adjusted for seasonal effects), whereas no such correlationswere found during 1994–2000 in the same population. Wesuggest that the earlier correlations were probably caused indirectlyby covariation with territory quality, and that a decline inpopulation size has changed the role of territory quality. Inthe Swedish population, an earlier study found a striking correlationbetween the size of a male's repertoire and the viability ofits offspring, suggesting good-gene effects. In contrast, wefound no such correlation in the German population, neitherin 1981–1982 nor in 1994–2000. We conclude thatrepertoire size does not seem to be a very reliable indicatorof variation in male quality. Interestingly, the analysis ofdata from 1994–2000 showed that male pairing success wasstrongly correlated with measures of strophe length and immediateversatility, traits that have been found to reflect male longevity.Future studies will have to show whether these performance-relatedtraits are more powerful indicators of male quality than isrepertoire size.     

Variation in growth in the blue tit (Parus caeruleus)

The pattern and amount of phenotypic and genetic variation in growth was analysed using the infinite-dimensional model in natural populations of the blue tit (Parus caeruleus). A size-index was used to analyse patterns of variation and covariation across ages (2, 5, 8, 11 and 14 days). Genetic variation was analysed using mother-, father-, and midparent-offspring regressions in the blue tit. Phenotypic variation in growth was limited to a few dimensions only, while heritabilities were close to zero at all ages except at 2 days when a significant mother-offspring relation was found. The phenotypic variance-covariance matrix over ages was found to be singular, which suggests that there are trajectories for which there is no phenotypic variation, and which therefore they cannot evolve. The phenotypic growth trajectory associated with the largest amount of variation basically showed a high to moderately high covariation across ages. These results have macroevolutionary implications in terms of the outcome of selection which generally will be in terms of overall size changes but with a slow rate of change due to low heritabilities; an outcome consistent with macro-evolutionary patterns of morphological variation in birds. A simulation study supported the conclusion that high covariances among traits and ages can impose considerable constraint on a microevolutionary scale.     

Intersexual niche differentiation in the blue tit (Parus caeruleus)

The intersexual niche differentiation hypothesis, according to which sexual size dimorphism (SSD) has evolved to facilitate niche separation between the sexes, has received equivocal support in studies of birds. One explanation for the inconsistency of the results is that other factors crucial for reproductive success, such as variation in food abundance among territories, may obscure food niche differentiation between parents. We studied the effects of SSD, food availability and food demands of broods on niche differentiation in the blue tit ( Parus caeruleus ). Parents attending experimentally enlarged broods delivered the same amount, but more diverse food items, to their offspring than parents attending reduced broods, although this effect was significant in only one of the two study years. The time-lag (deviation from the peak food abundance in habitat in days) and squared time-lag were the most important determinants of the diversity of food items delivered to young and their condition (fitness surrogate). SSD, as measured by principal component scores of morphological traits, did not explain any variation neither in the diversity or amount of food provided, nor in offspring condition. These results suggest that synchronization of breeding with peak food availability is the most important determinant of diversity of food delivered to young and, more importantly, Their condition. No evidence for intersexual food niche differentiation was found; at best, it is likely to constitute only a weak selection pressure on the maintenance or enhancement of SSD in this system.     

Fixed and dilutable benefits: female choice for good genes or fertility

Benefits accruing to females who exercise mate choice have been defined to be either 'direct' or 'indirect'. We suggest an alternative distinction: benefits can be considered 'fixed', meaning they are on average equal to all females mating with the same male (e.g. good genes' benefits) or 'dilutable', meaning they are shared between females mating with the same male, so that the more mates a male has, the lower the average benefit to each (e.g. fertility benefits or many forms of direct benefit). Using a simple model, we show that this distinction has a major effect on the form of female preference. We predict that mating skew will be far greater in species where the benefits are fixed when compared with those where the benefits are dilutable.     

The function of extrapair paternity in blue tits and great tits: good genes or fertility insurance?

DNA fingerprinting of an island population of blue tits andgreat tits in southeast Norway revealed that extrapair paternityaccounted for 36% (17/47) and 27% (15/55) of broods and for7% (31/466) and 8% (33/408) of young in the two species, respectively.Cuckolded males did not differ from noncuckolded males withrespect to morphology, age, or survival. There was no seasonalpattern in the frequency of extrapair paternity, and males showedno individual consistency in paternity loss over multiple broods.Extrapair offspring did not grow faster, they did not fledgewith a higher body mass, and they did not show a higher localsurvival rate than their half siblings. Hence, there was noevidence of any association between extrapair paternity andmale phenotypic or genotypic quality. Extrapair offspring wererandomly distributed among broods, with the only exceptionsof one blue tit and two great tit broods in which all young(six to nine) were sired by an extrapair male. This patternis best explained by a small proportion of males (2%–4%)being infertile and by most females performing a few extrapaircopulations as insurance against laying infertile eggs. We concludethat the results suggest a role for fertility insurance butthat alternative functional explanations to extrapair paternityin these populations cannot yet be ruled out.     

Local specialization and maladaptation in the Mediterranean blue tit (Parus caeruleus)

Although the evolutionary interplay between gene flow and local adaptation of organisms in heterogeneous environments has been widely discussed from a theoretical point of view, few empirical studies have been designed to test predictions on the consequences of habitat patchiness on the evolution of life history traits. Using blue tits in Mediterranean habitat mosaics as a model, we defined two nested levels of habitat heterogeneity: an inter-regional level which compares two isolated landscapes (mainland, southern France vs the island of Corsica), and an intra-regional level which compares two habitat types within each landscape (deciduous vs evergreen trees). Deciduous habitats are more common than evergreen habitats on the mainland whereas the opposite is true on the island. Results suggest that: (1) on a regional scale, each population is specialized to the more common habitat, i.e. life history traits have evolved in such a way that breeding success is high; (2) in the less common habitats within each landscape, birds are clearly mistimed because they mismatch the best period of food availability, and hence their breeding success is lower; and (3) the density of the populations and the morphometry of the birds support the model of ideal despotic distribution. These results, which are supported by preliminary data on the genetic variation and gene flow of populations in the mainland landscape, are consistent with a source-sink model of population structure within each landscape. They are discussed in the framework of metapopulation theory and habitat selection models.     

Courtship song, male agonistic encounters, and female mate choice in the house cricket,Acheta domesticus (Orthoptera: Gryllidae)

Whether female crickets choose among males based on characteristics of the courtship song is uncertain, but in many species, males not producing courtship song do not mate. In the house cricket,Acheta domesticus, we examined whether a female chose or rejected a male based on his size, latency to chirp, latency to produce courtship song, or rate of the high-frequency pulse of courtship song (“court rate”). We confirmed that females mated only with males that produced courtship song, but we found no evidence that the other factors we measured affected a female’s decision to mate. In addition, we investigated whether the outcome of male agonistic encounters affected the subsequent production of courtship song. In one experiment, we observed courtship and mating behavior when a single female was placed with a pair of males following a 10-min interaction period between the two males. Winners of male agonistic encounters had higher mating success. However, winners and losers of agonistic encounters were not different in their likelihood or latency to produce courtship song or in the number of times they were disrupted by the other male in the pair. In a second experiment, we allowed two males to interact for a 10-min period, but following this interaction period, we placed a female with each male separately and observed courtship and mating behavior. The mating success of winners and losers was not different under these circumstances, and we found no differences between winners and losers in any subsequent courtship or mating behavior examined. We conclude that winning agonistic encounters influences a male’s mating success in ways other than his production of courtship song and this effect is lost when winning and losing males are separated and each is given an opportunity to mate.     

The effect of male tenure and female mate choice on paternity in free-ranging Japanese macaques

In this study, the paternity of all the infants born in 2002 and 2003 in a free-ranging Japanese macaque (Macaca fuscata) group at Arashiyama in Kyoto, Japan, was analyzed in relation to males' age, dominance rank, and tenure and females' mate choice. The fathers of 20 out of 23 infants were determined by DNA analyses. Central adult (high-ranking) males sired two infants, whereas peripheral adult (low-ranking) males sired 14 infants. Young males sired only one infant. Among adult males, tenure was the most dominant factor that negatively affected male reproductive success. The mating behavior of females who gave birth was also analyzed. The number of male copulations in the peri-fertilization period was positively correlated with the number of infants that they sired. Females copulated with central males with a long tenure only when fertilization was unlikely or impossible. The females probably avoided insemination by males with a long tenure and selected males with a shorter tenure as their mating partners during the ovulation period.     

A spatial genetic structure and effects of relatedness on mate choice in a wild bird population

Inbreeding depression, as commonly found in natural populations, should favour the evolution of inbreeding avoidance mechanisms. If natal dispersal, the first and probably most effective mechanism, does not lead to a complete separation of males and females from a common origin, a small-scale genetic population structure may result and other mechanisms to avoid inbreeding may exist. We studied the genetic population structure and individual mating patterns in blue tits (Parus caeruleus). The population showed a local genetic structure in two out of four years: genetic relatedness between individuals (estimated from microsatellite markers) decreased with distance. This pattern was mainly caused by immigrants to the study area; these, if paired with fellow immigrants, were more related than expected by chance. Since blue tits did not avoid inbreeding with their social partner, we examined if individuals preferred less related partners at later stages of the mate choice process. We found no evidence that females or males avoided inbreeding through extra-pair copulations or through mate desertion and postbreeding dispersal. Although the small-scale genetic population structure suggests that blue tits could use a simple rule of thumb to select less related mates, females did not generally prefer more distantly breeding extra-pair partners. However, the proportion of young fathered by an extra-pair male in mixed paternity broods depended on the genetic relatedness with the female. This suggests that there is a fertilization bias towards less related copulation partners and that blue tits are able to reduce the costs of inbreeding through a postcopulatory process.     

Reliable acoustic cues for female mate preference in a katydid (Scudderia curvicauda, Orthoptera: Tettigoniidae)

The call of male Scudderia curvicauda (Orthoptera: Tettigoniidae)consists of a series of phrases, and each phrase contains syllables.Females respond to the male signal with ticks that follow malephrases after a specific period of time. Pair formation takesplace after males locate the female using her response sounds.Repeated recordings of males revealed that the average numberof syllables produced per phrase was a table, within-male parameterand that this parameter was a reliable predictor of male size(pronotum length). Thus, phrase length could be a reliable cueby which females evaluate males. We presented virgin femaleswith a sequential choice of two tape-recorded male calls thatdiffered only in the mean number of syllables produced per phrase.Two different playback tapes were used, and each female wastested on each of 5 consecutive days with the same playbacktape. Females responded more often and with a greater numberof ticks to calls containing more syllables per phrase, andthis preference was maintained throughout the testing period.Male size was a poor predictor of the size of the spermatophorefood-gift produced by the male; therefore, females are probablynot selecting males for this attribute. For one of the playbacktapes, there was a significant increase in female responsivenessover several playback trials, suggesting that females may employa falling-threshold tactic with respect to mate preference.     

Sexual conflict and cryptic female choice in the black field cricket, Teleogryllus commodus

The prevalence and evolutionary consequences of cryptic female choice (CFC) remain highly controversial, not least because the processes underlying its expression are often concealed within the female reproductive tract. However, even when female discrimination is relatively easy to observe, as in numerous insect species with externally attached spermatophores, it is often difficult to demonstrate directional CFC for certain male phenotypes over others. Using a biological assay to separate male crickets into attractive or unattractive categories, we demonstrate that females strongly discriminate against unattractive males by removing their spermatophores before insemination can be completed. This results in significantly more sperm being transferred by attractive males than unattractive males. Males respond to CFC by mate guarding females after copulation, which increases the spermatophore retention of both attractive and unattractive males. Interestingly, unattractive males who suffered earlier interruption of sperm transfer benefited more from mate guarding, and they guarded females more vigilantly than attractive males. Our results suggest that postcopulatory mate guarding has evolved via sexual conflict over insemination times rather than through genetic benefits of biasing paternity toward vigorous males, as has been previously suggested.