Social structure influences extra-pair paternity in socially monogamous mammals.
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ABSTRACT:
SUBMITTER: Cohas A
PROVIDER: S-EPMC2679913 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Previous work based on molecular evidence has shown that most socially monogamous birds follow a genetic polyandrous mating system. However, our knowledge about avian mating systems is heavily biased toward the north temperate zone, with data on tropical birds remaining relatively scarce. This uneven distribution of both phylogenetic and spatial sampling has hampered our understanding and interpretation of results. In this study, we investigated the frequency of extra-pair paternity (EPP) in a tropical population of yellow-bellied prinias ( Prinia flaviventris) in Guangxi, southern China. A total of 129 individuals belonging to 24 nests were sampled, among which 12 out of 83 chicks (14.46%) in seven nests were found to be EPP offspring. In nests in which all nestlings were sampled, only five out of 56 chicks were EPP offspring, accounting for an unbiased EPP rate of 8.93%. This rate is below the average rate of EPP in the family Sylviidae. The possible causes of EPP in prinias and the occurrence of EPP in birds with high resource investment and intensive parental care are discussed. This study highlights the value of genome-wide markers in determining relatedness in a wild bird species without a reference genome.
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Project description:When females copulate with multiple males, pre- and post-copulatory sexual selection may interact synergistically or in opposition. Studying this interaction in wild populations is complex and potentially biased, because copulation and fertilization success are often inferred from offspring parentage rather than being directly measured. Here, I simulated 15 species of socially monogamous birds with varying levels of extra-pair paternity, where I could independently cause a male secondary sexual trait to improve copulation success, and a sperm trait to improve fertilization success. By varying the degree of correlation between the male and sperm traits, I show that several common statistical approaches, including univariate selection gradients and paired t-tests comparing extra-pair males to the within-pair males they cuckolded, can give highly biased results for sperm traits. These tests should therefore be avoided for sperm traits in socially monogamous species with extra-pair paternity, unless the sperm trait is known to be uncorrelated with male trait(s) impacting copulation success. In contrast, multivariate selection analysis and a regression of the proportion of extra-pair brood(s) sired on the sperm trait of the extra-pair male (including only broods where the male sired ≥1 extra-pair offspring) were unbiased, and appear likely to be unbiased under a broad range of conditions for this mating system. In addition, I investigated whether the occurrence of pre-copulatory selection impacted the strength of post-copulatory selection, and vice versa. I found no evidence of an interaction under the conditions simulated, where the male trait impacted only copulation success and the sperm trait impacted only fertilization success. Instead, direct selection on each trait was independent of whether the other trait was under selection. Although pre- and post-copulatory selection strength was independent, selection on the two traits was positively correlated across species because selection on both traits increased with the frequency of extra-pair copulations in these socially monogamous species.
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Project description:Although many birds are socially monogamous, most (>75%) studied species are not strictly genetically monogamous, especially under high breeding density. We used molecular tools to reevaluate the reproductive strategy of the socially monogamous white stork (Ciconia ciconia) and examined local density effects. DNA samples of nestlings (Germany, Spain) were genotyped and assigned relationships using a two-program maximum likelihood classification. Relationships were successfully classified in 79.2% of German (n = 120) and 84.8% of Spanish (n = 59) nests. For each population respectively, 76.8% (n = 73) and 66.0% (n = 33) of nests contained only full-siblings, 10.5% (n = 10) and 18.0% (n = 9) had half-siblings (at least one nestling with a different parent), 3.2% (n = 3) and 10.0% (n = 5) had unrelated nestlings (at least two nestlings, each with different parents), and 9.5% (n = 9) and 6.0% (n = 3) had "not full-siblings" (could not differentiate between latter two cases). These deviations from strict monogamy place the white stork in the 59(th) percentile for extra-pair paternity among studied bird species. Although high breeding density generally increases extra-pair paternity, we found no significant association with this species' mating strategies. Thus although genetic monogamy is indeed prominent in the white stork, extra-pair paternity is fairly common compared to other bird species and cannot be explained by breeding density.
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Project description:In socially monogamous species, extra-pair paternity (EPP) is predicted to increase variance in male reproductive success (RS) beyond that resulting from genetic monogamy, thus, increasing the "opportunity for selection" (maximum strength of selection that can act on traits). This prediction is challenging to investigate in wild populations because lifetime reproduction data are often incomplete. Moreover, age-specific variances in reproduction have been rarely quantified. We analyzed 21 years of near-complete social and genetic reproduction data from an insular population of Seychelles warblers (Acrocephalus sechellensis). We quantified EPP's contribution to lifetime and age-specific opportunities for selection in males. We compared the variance in male genetic RS vs social ("apparent") RS (RSap ) to assess if EPP increased the opportunity for selection over that resulting from genetic monogamy. Despite not causing a statistically significant excess (19%) of the former over the latter, EPP contributed substantially (27%) to the variance in lifetime RS, similarly to within-pair paternity (WPP, 39%) and to the positive WPP-EPP covariance (34%). Partitioning the opportunity for selection into age-specific (co)variance components, showed that EPP also provided a substantial contribution at most ages, varying with age. Therefore, despite possibly not playing the main role in shaping sexual selection in Seychelles warblers, EPP provided a substantial contribution to the lifetime and age-specific opportunity for selection, which can influence evolutionary processes in age-structured populations.
| S-EPMC9322416 | biostudies-literature
Project description:Female extra-pair reproduction in socially monogamous systems is predicted to cause cuckolded socially-paired males to conditionally reduce paternal care, causing selection against extra-pair reproduction and underlying polyandry. However, existing models and empirical studies have not explicitly considered that cuckolded males might be related to their socially-paired female and/or to her extra-pair mate, and therefore be related to extra-pair offspring that they did not sire but could rear. Selection against paternal care, and hence against extra-pair reproduction, might then be weakened. We derive metrics that quantify allele-sharing between within-pair and extra-pair offspring and their mother and her socially-paired male in terms of coefficients of kinship and inbreeding. We use song sparrow (Melospiza melodia) paternity and pedigree data to quantify these metrics, and thereby quantify the joint effects of extra-pair reproduction and inbreeding on a brood's total allelic value to its socially-paired parents. Cuckolded male song sparrows were almost always detectably related to extra-pair offspring they reared. Consequently, although brood allelic value decreased substantially following female extra-pair reproduction, this decrease was reduced by within-pair and extra-pair reproduction among relatives. Such complex variation in kinship within nuclear families should be incorporated into models considering coevolutionary dynamics of extra-pair reproduction, parental care, and inbreeding.
| S-EPMC4949684 | biostudies-literature
Project description:Since the first molecular study providing evidence for mating outside the pair bond in birds over 30 years ago, >500 studies have reported rates of extra-pair paternity (EPP) in >300 bird species. Here, we give a detailed overview of the current literature reporting EPP in birds and highlight the sampling biases and patterns in the data set with respect to taxonomy, avian phylogeny and global regions, knowledge of which will be crucial for correct interpretation of results in future comparative studies. Subsequently, we use this comprehensive dataset to simultaneously test the role of several ecological and life history variables. We do not find clear evidence that variation in EPP across socially monogamous species can be explained by latitude, density (coloniality), migration, generation length, genetic structuring (dispersal distance), or climatic variability, after accounting for phylogeny. These results contrast previous studies, most likely due to the large heterogeneity within species in both EPP and the predictor of interest, indicating that using species averages might be unreliable. Despite the absence of broadscale ecological drivers in explaining interspecific variation in EPP, we suggest that certain behaviours and ecological variables might facilitate or constrain EPP, as indicated by our finding that EPP was negatively associated with latitude within noncolonial species, suggesting a role of breeding synchrony. Thus, rather than focussing on general explanations for variation in EPP across all species, a future focus should be on how various aspects of ecology or life history might have driven variation in EPP among groups of species or populations of the same species. Hence, we argue that variation in EPP can be partly explained when taking the right perspective. This comprehensive overview, and particularly the dataset provided herein will create a foundation for further studies.
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Project description:Pair-bonded primates have uniquely enduring relationships and partners engage in a suite of behaviors to maintain these close bonds. In titi monkeys, pair bond formation has been extensively studied, but changes across relationship tenure remain unstudied. We evaluated differences in behavioral indicators of pair bonding in newly formed (~6 months paired, n = 9) compared to well-established pairs (average 3 years paired, n = 8) of titi monkeys (Callicebus cupreus) as well as sex differences within the pairs. We hypothesized that overall males would contribute more to maintenance than females, but that the pattern of maintenance behaviors would differ between newly formed and well-established pairs. Each titi monkey (N = 34) participated in a partner preference test (PPT), where the subject was placed in a middle test cage with grated windows separating the subject from the partner on one side and an opposite-sex stranger on the other side. During this 150-min behavioral test, we quantified four key behaviors: time in proximity to the partner or stranger as well as aggressive displays toward the partner or stranger. Overall, we found different behavioral profiles representing newly formed and well-established pair-bond relationships in titi monkeys and male-biased relationship maintenance. Males spent ∼40% of their time in the PPT maintaining proximity to the female partner, regardless of relationship tenure. Males from well-established bonds spent less time (14%) near the female stranger compared to males from newly formed bonds (21%) at the trend level. In contrast, females from well-established bonds spent less (23%) time near the male partner in the PPT compared to females from newly formed bonds (47%). Aggressive displays were more frequent in newly formed bonds compared to well-established bonds, especially for females. Scan sampling for homecage affiliation showed that newly formed pairs were more likely to be found tail twining than well-established pairs.
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Project description:Extra-group paternity (EGP) can form an important part of the mating system in birds and mammals. However, our present understanding of its extent and ecology comes primarily from birds. Here, we use data from 26 species and phylogenetic comparative methods to explore interspecific variation in EGP in mammals and test prominent ecological hypotheses for this variation. We found extensive EGP (46% of species showed more than 20% EGP), indicating that EGP is likely to play an important role in the mating system and the dynamics of sexual selection in mammals. Variation in EGP was most closely correlated with the length of the mating season. As the length of the mating season increased, EGP declined, suggesting that it is increasingly difficult for males to monopolize their social mates when mating seasons are short and overlap among females in oestrus is likely to be high. EGP was secondarily correlated with the number of females in a breeding group, consistent with the idea that as female clustering increases, males are less able to monopolize individual females. Finally, EGP was not related to social mating system, suggesting that the opportunities for the extra-group fertilizations and the payoffs involved do not consistently vary with social mating system.
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Project description:Extra-pair paternity is the result of copulation between a female and a male other than her social partner. In socially monogamous birds, old males are most likely to sire extra-pair offspring. The male manipulation and female choice hypotheses predict that age-specific male mating behaviour could explain this old-over-young male advantage. These hypotheses have been difficult to test because copulations and the individuals involved are hard to observe. Here, we studied the mating behaviour and pairing contexts of captive house sparrows, Passer domesticus. Our set-up mimicked the complex social environment experienced by wild house sparrows. We found that middle-aged males, which would be considered old in natural populations, gained most extra-pair paternity. However, both, female solicitation behaviour and subsequent extra-pair matings were not associated with male age. Further, copulations were more likely when solicited by females than when initiated by males (i.e. unsolicited copulations). Male initiated within-pair copulations were more common than male initiated extra-pair copulations. To conclude, our results did not support either hypothesis regarding age-specific male mating behaviour. Instead, female choice, independent of male age, governed copulation success, especially in an extra-pair context. Post-copulatory mechanisms might determine why older males sire more extra-pair offspring.
| S-EPMC5976671 | biostudies-literature
Project description:Although the majority of passerine birds are socially monogamous, true genetic monogamy is rare, with extra-pair paternity (EPP) occurring in almost 90% of surveyed socially monogamous species. We present the first molecular data on the genetic breeding system of the long-tailed finch, Poephila acuticauda, a grass finch endemic to the tropical northern savannah of Australia. Although the species forms socially monogamous pair bonds during the breeding season, we found that extra-pair males sired 12.8% of 391 offspring, in 25.7% of 101 broods. Our findings provide only the second estimate of extra-pair paternity in the estrildid finch family.
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