Genetic covariance between components of male reproductive success: within‐pair vs. extra‐pair paternity in song sparrows

Abstract Although polygyny can potentially increase male reproductive success, the benefits of this strategy could be offset by losses to extra-pair paternity or reduced offspring survival. We developed microsatellite markers to assess the influence of extra-pair offspring (EPO) on reproductive success and paternity in monogamous and polygynous pairs of the facultatively polygynous Southwestern Willow Flycatcher (Empidonax traillii extimus). Based on genotypes of 140 offspring from 56 clutches over six years, 14% of nestlings in our study population were extra-pair offspring, with 23% of all successful nests containing at least one EPO. We found that polygynous males produced 2.11 ± 0.35 offspring per season, compared to 1.15 ± 0.18 for monogamous males. This increased reproductive success was due primarily to the increased number of nests of polygynous males, as the number of offspring per pair did not differ between monogamous and polygynous males. Twenty of the 140 genotyped nestlings were extra-pair offspring. Sires could be assigned to 16 of these; one polygynous male sired two EPO in one nest, two monogamous males sired eight EPO in two nests, and four nonterritorial males sired six EPO in four nests. Overall, these results indicate that in this population, females of polygynous males did not raise a disproportionate number of EPO as a result of the polygynous mating strategy of their mate, and that both territorial and nonterritorial males sired EPO.

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Single-locus DNA fingerprinting reveals that male reproductive success increases with age through extra-pair paternity in the house sparrow ( Passer domesticus )

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.1995.0064 ◽

1995 ◽

Vol 260 (1357) ◽

pp. 91-98 ◽

Cited By ~ 82

Keyword(s):

Reproductive Success ◽

Dna Fingerprinting ◽

House Sparrow ◽

Passer Domesticus ◽

Single Locus ◽

Male Reproductive Success ◽

Extra Pair Paternity

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Postweaning maternal care increases male chimpanzee reproductive success

Science Advances ◽

10.1126/sciadv.aaz5746 ◽

2020 ◽

Vol 6 (38) ◽

pp. eaaz5746

Author(s):

Catherine Crockford ◽

Liran Samuni ◽

Linda Vigilant ◽

Roman M. Wittig

Keyword(s):

Reproductive Success ◽

Parental Investment ◽

Maternal Care ◽

Parental Loss ◽

Male Reproductive Success ◽

Complex Societies ◽

Successful Reproduction ◽

Using Data

Humans are unusual among animals for continuing to provision and care for their offspring until adulthood. This “prolonged dependency” is considered key for the evolution of other notable human traits, such as large brains, complex societies, and extended postreproductive lifespans. Prolonged dependency must therefore have evolved under conditions in which reproductive success is gained with parental investment and diminished with early parental loss. We tested this idea using data from wild chimpanzees, which have similarly extended immature years as humans and prolonged mother-offspring associations. Males who lost their mothers after weaning but before maturity began reproducing later and had lower average reproductive success. Thus, persistent mother-immature son associations seem vital for enhancing male reproductive success, although mothers barely provision sons after weaning. We posit that these associations lead to social gains, crucial for successful reproduction in complex social societies, and offer insights into the evolution of prolonged dependency.

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Male reproductive success and sexual selection in northern water snakes determined by microsatellite DNA analysis

Behavioral Ecology ◽

10.1093/beheco/13.6.808 ◽

2002 ◽

Vol 13 (6) ◽

pp. 808-815 ◽

Cited By ~ 25

Author(s):

P. J. Weatherhead

Keyword(s):

Sexual Selection ◽

Reproductive Success ◽

Microsatellite Dna ◽

Dna Analysis ◽

Male Reproductive Success ◽

Northern Water Snakes ◽

Water Snakes

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POLYGYNY, REPRODUCTIVE SUCCESS AND CHILD HEALTH IN RURAL ETHIOPIA: WHY MARRY A MARRIED MAN?

Journal of Biosocial Science ◽

10.1017/s0021932006001441 ◽

2006 ◽

Vol 39 (2) ◽

pp. 287-300 ◽

Cited By ~ 61

Author(s):

MHAIRI A. GIBSON ◽

RUTH MACE

Keyword(s):

Reproductive Success ◽

Male Reproductive Success ◽

Family Status ◽

Rural Ethiopia ◽

Younger Age ◽

Married Individuals ◽

Males And Females ◽

Child Nutritional Status ◽

And Child Health ◽

Better Than

Summary.This study examines the reproductive success of men and women in rural Ethiopia as a function of their marital status, specifically by comparing polygamously and monogamously married individuals. In line with predictions from evolutionary theory, polygamy is beneficial to male reproductive success (i.e. producing larger numbers of surviving offspring). The success of polygamously married females depends on wife rank: the first wives of polygamous husbands do better than monogamously married women and much better than second or third wives. These effects are mirrored in child nutritional status: the children of second and third wives have lower weight for height. Due to potential, largely unmeasurable differences in marriageability (quality) between individuals, it was not possible to support a model of either resource-holding polygyny combined with female choice or female coercion into unwanted marriages. First wives of polygamously married men marry at a younger age and attract a higher brideprice, suggesting that both the males and females in the marriage are likely to be of higher quality (due to wealth, family status or some other factor such as beauty). Unions that end up monogamous are likely to be between slightly lower quality individuals; and second and third wives, who marry at the oldest ages and attract the lowest brideprice, may be ‘making the best of a bad job’. The relatively long gap between first and second marriages may mean that first wives of highly marriageable males can enjoy considerable reproductive success before their husbands marry again.

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Carotenoid-based plumage colouration in red bishops (Euplectes orix) — signalling presence rather than quality?

Behaviour ◽

10.1163/000579511x608693 ◽

2011 ◽

Vol 148 (11-13) ◽

pp. 1372-1392 ◽

Cited By ~ 3

Author(s):

Alice U. Edler ◽

Thomas W.P. Friedl

Keyword(s):

Reproductive Success ◽

Parasite Load ◽

Blood Parasite ◽

Male Reproductive Success ◽

Sexually Dimorphic ◽

Male Quality ◽

Plumage Colouration ◽

Selection For ◽

Breeding Plumage

AbstractThe role of bright plumage colouration for female choice has been the focus of research in sexual selection for many years, with several studies showing that females prefer the most elaborately ornamented males, which are often also the highest quality individuals. Here, we analysed the associations between reproductive performance and plumage, body condition and blood parasite load in the red bishop (Euplectes orix), a sexually dimorphic and polygynous weaverbird species, where males in a carotenoid-based orange-to-red breeding plumage defend territories and build many nests to which they try to attract females. Male reproductive success in terms of number of nests accepted was mainly determined by the number of nests built, but was also positively related to blood parasite load, while we found no influence of plumage characteristics. Together with previously obtained data, our results indicate that plumage characteristics in the red bishop do not affect male reproductive success and are generally not suitable to reliably indicate male quality. We suggest that the primary function of the brilliant orange-scarlet breeding plumage might be presence signalling in terms of increasing conspicuousness of breeding males to females searching for mates.

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Variation in reproductive success of male and female Columbian ground squirrels (Urocitellus columbianus)

Canadian Journal of Zoology ◽

10.1139/z2012-042 ◽

2012 ◽

Vol 90 (6) ◽

pp. 736-743 ◽

Cited By ~ 5

Author(s):

Philip H. Jones ◽

Jeffrey L. Van Zant ◽

F. Stephen Dobson

Keyword(s):

Reproductive Success ◽

Mating System ◽

Multiple Paternity ◽

Ground Squirrels ◽

Male Reproductive Success ◽

Offspring Production ◽

Bateman Gradient ◽

Coefficients Of Variation ◽

Males And Females ◽

Columbian Ground Squirrels

The imbalanced reproductive success of polygynous mammals results in sexual selection on male traits like body size. Males and females might have more balanced reproductive success under polygynandry, where both sexes mate multiply. Using 4 years of microsatellite DNA analyses of paternity and known maternity, we investigated variation in reproductive success of Columbian ground squirrels, Urocitellus columbianus (Ord, 1815); a species with multiple mating by both sexes and multiple paternity of litters. We asked whether male reproductive success was more variable than that of females under this mating system. The overall percentage of confirmed paternity was 61.4% of 339 offspring. The mean rate of multiple paternity in litters with known fathers was 72.4% (n = 29 litters). Estimated mean reproductive success of males (10.27 offspring) was about thrice that of females (3.11 offspring). Even after this difference was taken into account statistically, males were about three times as variable in reproductive success as females (coefficients of variation = 77.84% and 26.74%, respectively). The Bateman gradient (regression slope of offspring production on number of successful mates) was significantly greater for males (βM = 1.44) than females (βF = 0.28). Thus, under a polygynandrous mating system, males exhibited greater variation in reproductive success than females.

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Female, but not male, agonistic behaviour is associated with male reproductive success in stable bluebanded goby (Lythrypnus dalli) hierarchies

Behaviour ◽

10.1163/1568539x-00003188 ◽

2014 ◽

Vol 151 (10) ◽

pp. 1367-1387 ◽

Cited By ~ 13

Author(s):

Tessa K. Solomon-Lane ◽

Madelyne C. Willis ◽

Devaleena S. Pradhan ◽

Matthew S. Grober

Keyword(s):

Reproductive Success ◽

Egg Laying ◽

Dominant Male ◽

Male Reproductive Success ◽

Agonistic Behaviour ◽

Social Species ◽

Evolution Of Sociality ◽

Lythrypnus Dalli ◽

Linear Hierarchies ◽

Substantial Control

In many social species, there are important connections between social behaviour and reproduction that provide critical insights into the evolution of sociality. In this study, we describe associations between agonistic behaviour and male reproductive success in stable social groups of bluebanded gobies (Lythrypnus dalli). This highly social, sex-changing species forms linear hierarchies of a dominant male and multiple subordinate females. Males reproduce with each female in the harem and care for the eggs. Since aggression tends to be associated with reduced reproduction in social hierarchies, we hypothesized that males in groups with high rates of aggression would fertilise fewer eggs. We also hypothesized that a male’s agonistic behaviour would be associated with his reproductive success. Dominants often exert substantial control over their harem, including control over subordinate reproduction. To address these hypotheses, we quantified egg laying/fertilisation over 13 days and observed agonistic behaviour. We show that there was a significant, negative association between male reproductive success and the total rate agonistic interactions by a group. While no male behaviours were associated with the quantity of eggs fertilised, female agonistic behaviour may be central to male reproductive success. We identified a set of models approximating male reproductive success that included three female behaviours: aggression by the highest-ranking female and approaches by the lowest-ranking female were negatively associated with the quantity of eggs fertilised by males in their groups, but the efficiency with which the middle-ranking female displaced others was positively associated with this measure. These data provide a first step in elucidating the behavioural mechanisms that are associated with L. dalli reproductive success.

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Individual Variation in the Strength of Territory Defense in Male Song Sparrows: Correlates of Age, Territory Tenure, and Neighbor Aggressiveness

Behaviour ◽

10.1163/156853904772746574 ◽

2004 ◽

Vol 141 (1) ◽

pp. 15-27 ◽

Cited By ~ 60

Author(s):

Jeremy Hyman ◽

Melissa Hughes ◽

Stephen Nowicki ◽

William Searcy

Keyword(s):

Individual Differences ◽

Reproductive Success ◽

Extrinsic Factors ◽

Territory Defense ◽

Intrinsic Factors ◽

Territorial Aggression ◽

Male Song ◽

Song Sparrows ◽

Territory Owner ◽

Older Males

AbstractIn many species, the ability to defend a territory is essential for a male to obtain any reproductive success at all, and even among territorial individuals, variation in the strength of territory defense could have a significant impact on how much reproductive success is obtained. Previous studies have documented consistent individual differences in the vigor with which male song sparrows (Melospiza melodia) defend their territories, as measured by the strength of their reactions to territorial intrusions simulated through song playback. Variation in the strength of defense could reflect intrinsic differences among individuals in their resource holding potential (RHP), or variation in extrinsic factors. In this study, we examined whether variation in the strength of territory defense corresponds to differences in intrinsic factors such as the age or experience of the territory owner, the extrinsic factor of the level of aggression shown by neighbours, or both. Results indicate that males that previously held territories on the study site, regardless of whether they were holding the same territory as the previous year, show higher levels of territory defense than males that are new to the study site, and, assuming that returning males are older males, suggest that age is more important than experience on a specific territory in determining strength of territory defense. In addition, we found evidence that males with high levels of territorial aggression tend to be spatially clustered. The pattern observed suggests that a combination of intrinsic and extrinsic factors contribute to the expression of individual differences in territorial aggression.

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The measure and significance of Bateman's principles

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2013.2973 ◽

2014 ◽

Vol 281 (1782) ◽

pp. 20132973 ◽

Cited By ~ 50

Author(s):

Julie M. Collet ◽

Rebecca F. Dean ◽

Kirsty Worley ◽

David S. Richardson ◽

Tommaso Pizzari

Keyword(s):

Reproductive Success ◽

Mating Success ◽

Male Reproductive Success ◽

Female Fecundity ◽

Male Preference ◽

Bateman Gradient ◽

Red Junglefowl ◽

Experimental Approaches ◽

Empirical Tests ◽

Paternity Share

Bateman's principles explain sex roles and sexual dimorphism through sex-specific variance in mating success, reproductive success and their relationships within sexes (Bateman gradients). Empirical tests of these principles, however, have come under intense scrutiny. Here, we experimentally show that in replicate groups of red junglefowl, Gallus gallus , mating and reproductive successes were more variable in males than in females, resulting in a steeper male Bateman gradient, consistent with Bateman's principles. However, we use novel quantitative techniques to reveal that current methods typically overestimate Bateman's principles because they (i) infer mating success indirectly from offspring parentage, and thus miss matings that fail to result in fertilization, and (ii) measure Bateman gradients through the univariate regression of reproductive over mating success, without considering the substantial influence of other components of male reproductive success, namely female fecundity and paternity share. We also find a significant female Bateman gradient but show that this likely emerges as spurious consequences of male preference for fecund females, emphasizing the need for experimental approaches to establish the causal relationship between reproductive and mating success. While providing qualitative support for Bateman's principles, our study demonstrates how current approaches can generate a misleading view of sex differences and roles.

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