Sexual selection,germline mutation rate and sperm competition

Background  

An important component of sexual selection arises because females obtain viability benefits for their offspring from their mate choice. Females choosing extra-pair fertilization generally favor males with exaggerated secondary sexual characters, and extra-pair paternity increases the variance in male reproductive success. Furthermore, females are assumed to benefit from 'good genes' from extra-pair sires. How additive genetic variance in such viability genes is maintained despite strong directional selection remains an evolutionary enigma. We propose that sexual selection is associated with elevated mutation rates, changing the balance between mutation and selection, thereby increasing variance in fitness and hence the benefits to be obtained from good genes sexual selection. Two hypotheses may account for such elevated mutation: (1) Increased sperm production associated with sperm competition may increase mutation rate. (2) Mutator alleles increase mutation rates that are revealed by the expression of condition-dependent secondary sexual characters used by choosy females during their mate choice. M Petrie has independently developed the idea that mutator alleles may account for the maintenance of genetic variation in viability despite strong directional selection.     

THE EVOLUTION OF PLUMAGE BRIGHTNESS IN BIRDS IS RELATED TO EXTRAPAIR PATERNITY

A positive association between plumage brightness of male birds and the degree of polygyny may be the result of sexual selection. Although most birds have a socially monogamous mating system, recent paternity analyses show that many offspring are fathered by nonmates. Extrapair paternity arises from extrapair copulations which are frequently initiated by females. Not all females will be able to mate with a male of the preferred phenotype, because of the mating decisions of earlier paired females; extrapair copulations may be a means for females to adjust their precopulation mate choice. We use two comparative analyses (standardized linear contrasts and pairwise comparisons between closely related taxa) to test the idea that male plumage brightness is related to extrapair paternity. Brightness of male plumage and sexual dimorphism in brightness were positively associated with high levels of extrapair paternity, even when potentially confounding variables were controlled statistically. This association between male brightness and extrapair paternity was considerably stronger than the association between male brightness and the degree of polygyny. Cuckoldry thus forms an important component of sexual selection in birds.     

Part-Time Mate Guarding Affects Paternity in Male Reed Buntings (Emberiza schoeniclus)

Male mate guarding by close following has been reported in many socially monogamous bird species and is generally believed to function as a paternity guard. Many aspects of the dynamics and effectiveness of this behavior are still however poorly understood. Here, we describe the temporal variation in mate guarding behavior in male reed buntings (Emberiza schoeniclus) with a particular focus on how males allocate their mating effort between mate guarding and extrapair mating in a context of intense sperm competition. In our highly synchronous study population most males have to balance the simultaneous and mutually exclusive demands of mate guarding and seeking extrapair copulations (EPCs). We found that males frequently switched between guarding their mates and performing intrusions to neighboring territories. Both activities seemed to have significant fitness payoffs, as male mate guarding effort had a positive effect on paternity, and a large fraction of extrapair fertilizations occurred during the days when the sire guarded its own female. The reed bunting is thus an example of how discontinuous or part‐time mate guarding can still be effective in securing paternity. Female reed buntings were not particularly active in initiating EPCs as they never were observed performing extraterritorial forays. We argue that the absence of female‐initiated EPCs is a prerequisite for males to trade mate guarding against seeking EPCs. Otherwise, if females circumvent male mate guarding by timing their EPCs to periods of male absence, males should guard their mates almost continuously or rely on alternative paternity guards.     

Extrapair paternity as a cost of polygyny in the rock sparrow: behavioural and genetic evidence of the ‘trade-off’ hypothesis

We studied the association between extrapair paternity (EPP) rate and male mating status in the rock sparrow, Petronia petronia, a facultative polygynous species. Overall, 32.0% (58/181) of the chicks were not sired by the social father and 57.1% (24/42) of the broods contained at least one extrapair young. Polygynous males allocated less time to guarding their mate during her fertile period than monogamous males but did not differ in the time spent guarding their nest. Polygynous males were cuckolded more frequently than monogamous males (50.5 and 6.6% of the young, respectively) and their paternity loss was positively correlated with the degree of overlap between the fertile periods of their primary and secondary females. Paternity loss did not differ between primary and secondary broods of polygynous males and acquiring a second mate was possible only at the expense of paternity in both broods. Late broods contained fewer extrapair young, despite no significant seasonal trend in the time allocated by the male to guarding his mate. Male yellow badge size was not associated with paternity. Old males were cuckolded less frequently than first-year males, but male age had a minor effect on paternity compared with male mating status. Reproductive success (number of young fledged/year) did not differ between monogamous and polygynous males once paternity was accounted for. Together, these results suggest that mate guarding can be efficient in preventing cuckoldry, and that there is a trade-off between attracting an additional mate and protecting paternity in the rock sparrow, whereas male age and phenotype were, at best, fair predictors of paternity. Copyright 2002 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour     

Parentage in the cooperative breeding system of long-tailed tits, Aegithalos caudatus

In cooperatively breeding birds multiple maternity and paternity of broods is not uncommon, reproduction often being shared among group members as well as with extragroup members. We investigated the extent of extrapair paternity and intraspecific brood parasitism in a population of cooperatively breeding long-tailed tits. Our aim was to determine the frequency and cause of mixed parentage and to investigate whether shared maternity or paternity was associated with decisions made by helpers. Genetic analyses using eight microsatellite loci showed that extrapair paternity was low (2.4-6.9% of nestlings in 16-29% of broods), and that intraspecific brood parasitism was negligible. Mate switching and extrapair copulations were both observed, but mate switching was not responsible for the mixed paternity we recorded. Some extrapair offspring were assigned to males that became helpers at the nest containing their extrapair young, but these males were also close neighbours of the cuckolded males and so were the most likely males to gain extrapair paternity. There was no evidence that the existence of a direct reproductive stake in a brood played an important role in the helping decisions of either male or female helpers. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Mate guarding, male attractiveness, and paternity under social monogamy

Socially monogamous species vary widely in the frequency ofextrapair offspring, but this is usually discussed assumingthat females are free to express mate choice. Using game-theorymodeling, we investigate the evolution of male mate guarding,and the relationship between paternity and mate-guarding intensity.We show that the relationship between evolutionarily stablemate-guarding behavior and the risk of cuckoldry can be complicatedand nonlinear. Because male fitness accumulates both throughpaternity at his own nest and through his paternity elsewhere,males evolve to guard little either if females are very faithfulor if they are very unfaithful. Attractive males are usuallyexpected to guard less than unattractive males, but within-pairpaternity may correlate either positively or negatively withthe number of extrapair offspring fertilized by a male. Negativecorrelations, whereby attractive males are cuckolded more, becomemore likely if the reason behind female extrapair behavior appliesto most females (e.g., fertility insurance) rather than thesubset mated to unattractive males (e.g., when females seek"good genes") and if mate guarding is efficient in controllingfemale behavior. We discuss the current state of empirical knowledgewith respect to these findings.     

Strategic paternity assurance in the sex-role reversed Eurasian dotterel (Charadrius morinellus): behavioral and genetic evidence

Sex role reversal in birds is usually associated with paternalcare of both eggs and chicks. This pattern of care typicallyleads to the potential rate of reproduction of males being lowerthan that of females. Hence, operational sex-ratio theory predictsthat each male should be under strong selection to avoid beingcuckolded. A male should, therefore, guard his female partner(s)from extrapair copulation attempts by other males. Furthermore,the sexual conflict theory of copulation behavior predicts thatin species with extensive paternal care the male should controlthe temporal pattern of copulations—copulations shouldoccur both frequently and throughout the prelaying period. Wetested these predictions in the Eurasian dotterel (Charadriusmorinsllus), in which the male usually provides all the parentalcare. In accordance with the first prediction, male dotterelsdid "guard" their pair-female prior to egg-laying. Contraryto the second prediction, however, copulations were not frequentand did not occur throughout the pre-laying phase-despite frequentsolicitation by the female, copulations only occurred immediatelyprior to egg-laying. Nevertheless, male-initiated courtshipwas both coincident with the pattern of copulations and morelikely than female-initiated courtship to result in copulation.Our results do, therefore, appear to agree with the centralprediction of the sexual conflict theory that males should controlthe pattern of copulations. We suggest that male dotterels willcopulate only after several days of being paired because theyface a duel risk of cuckoldry from both extrapair copulationand rapid mate switching. We tested the realized incidence ofcuckoldry using DNA fingerprinting. Only 4.6% (2/44) of chickswere not the genetic offspring of the caring male correspondingto 9.1% (2/22) broods affected. The rate of extrapair paternityin the dotterel is, therefore, relatively low compared to thatin many other avian species. We conclude that male dotterelssuccessfully protect their paternity of the brood for whichthey care through a combined strategy of mate guarding and strategictiming of copulations.     

Male phenotype predicts insemination success in guppies

Theory predicts that mate choice can lead to an increase in female fecundity if the secondary sexual traits used by females to assess male quality covary with the number of sperm transferred during copulation. Where females mate multiply, such a relationship between male attractiveness and ejaculate size may, additionally (or alternatively), serve to augment the effect of indirect selection by biasing paternity in favour of preferred males. In either case, a positive correlation between male attractiveness and the size of ejaculates delivered at copulation is predicted. To date, some of the most convincing (indirect) evidence for this prediction comes from the guppy, a species of fish exhibiting a resource-free mating system in which attractive males tend to have larger sperm reserves. We show that, during solicited copulations, male guppies with preferred phenotypes actually transfer more sperm to females than their less-ornamented counterparts, irrespective of the size of their initial sperm stores. Our results also reveal that, during coercive copulations, the relationship between ejaculate size and the male's phenotype breaks down. This latter result, in conjunction with our finding that mating speed--a factor under the female's control-is a significant predictor of ejaculate size, leads us to speculate that females may exert at least partial control over the number of sperm inseminated during cooperative matings.     

Maintenance of sperm variation in a highly promiscuous wild bird

Postcopulatory sexual selection is an important force in the evolution of reproductive traits, including sperm morphology. In birds, sperm morphology is known to be highly heritable and largely condition-independent. Theory predicts, and recent comparative work corroborates, that strong selection in such traits reduces intraspecific phenotypic variation. Here we show that some variation can be maintained despite extreme promiscuity, as a result of opposing, copulation-role-specific selection forces. After controlling for known correlates of siring success in the superb fairy-wren (Malurus cyaneus), we found that (a) lifetime extra-pair paternity success was associated with sperm with a shorter flagellum and relatively large head, and (b) males whose sperm had a longer flagellum and a relatively smaller head achieved higher within-pair paternity. In this species extrapair copulations occur in the same morning, but preceding, pair copulations during a female's fertile period, suggesting that shorter and relatively larger-headed sperm are most successful in securing storage (defense), whereas the opposite phenotype might be better at outcompeting stored sperm (offense). Furthermore, since cuckolding ability is a major contributor to differential male reproductive output, stronger selection on defense sperm competition traits might explain the short sperm of malurids relative to other promiscuous passerines.     

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.     

Intense extrapair behaviour in a semicolonial passerine does not result in extrapair fertilizations

Sperm competition is a strong force on the evolution of mating behaviour of animals, particularly birds. In monogamous birds extrapair behaviour is one main source of variation in the reproductive success of males, which has caused the evolution of paternity guards as well as strategies by females to increase the genetic quality of their descendants. We investigated the importance of sperm competition in the reproductive behaviour of serins, Serinus serinus. Male serins guarded their mates and also copulated frequently, indicating that sperm competition has been an important selective force affecting their mating behaviour. Females were frequently approached and chased by extrapair males that attempted extrapair copulations. However, females refused almost every attempt by extrapair males. No extrapair paternity was detected in the population, in spite of the intense extrapair behaviour of males. This supports the view that females keep strong control over paternity, and that in this population they do not seem to obtain genetic benefits from extrapair copulations. We discuss why the presence of high levels of sexual competition may not be reflected in extrapair paternity. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Extrapair paternity in the Hoopoe Upupa epops: an exploration of the influence of interactions between breeding pairs, non-pair males and strophe length

Previous studies of the Hoopoe Upupa epops have shown that the strophe length of male songs influences female mate choice, and is correlated with female reproductive rates and male production of fledglings in the male’s own brood. However, frequent interactions between breeding pairs and non‐pair males suggests that extrapair copulations could occur and could affect the real number of fledglings sired by males, and therefore the relationship between strophe length and breeding success. Here we analyse the incidence of interactions between breeding pairs and non‐pair males, and of extrapair paternity, the interrelation of these parameters, the influence of male strophe length on them, and whether extrapair fertilizations affect the correlation between strophe length and breeding success of males, in a colour‐ringed population of Hoopoes in south‐eastern Spain. Multilocus DNA‐fingerprinting revealed that 10% of the broods contained offspring sired by extrapair males, representing 7.7% of the chicks. However, the interactions between pairs and non‐pair males were more frequent, with more than 25% of broods being visited by non‐pair males, and about 10% being helped (fed or defended) by males other than the nest owner. Most of these relationships were apparently attempts by visitor males to obtain copulations with paired females, or to obtain access to such females or nests in future breeding attempts. However, there was no significant link between the detection of interactions with alien males in a nest and the occurrence of extrapair paternity in it, indeed extrapair paternity was found in only 30% of the nests with interactions, and therefore the detection of visits or helping by non‐pair males cannot be considered evidence of extrapair paternity in visited or helped broods. Males that sang with long strophes never suffered losses of paternity within their broods, while 25% of males that sang with short strophes did. However, these differences were not significant. Nevertheless, strophe length of males was significantly positively correlated with per brood and seasonal production of fledglings after accounting for losses of paternity within their own broods.     

Pre‐ and postcopulatory sexual selection act in concert to determine male reproductive success in Tribolium castaneum

To capture how sexual selection shapes male reproductive success across different stages of reproduction in Tribolium castaneum (Coleoptera, Tenebrionidae), we combined sequential sperm defence (P1) and sperm offence (P2) trials with additional trials where both males were added simultaneously to the female. We found a positive correlation between the relative paternity share in simultaneous male–male competition trials and the P2 trial. This suggests that males preferred by females as sires achieve superior fertilization success during sperm competition in the second male position. In simultaneous male–male competition trials, where pre‐, peri‐ and postcopulatory sexual selection were all allowed to act, the relative paternity share of preferred males was more than 20% higher than in P2 sperm competition trials where precopulatory female choice was disabled. Additional behavioural observations revealed that mating with more attractive males resulted significantly more frequently in offspring production than mating with less attractive males. Thus, by comparing male fertilization success in trials where precopulatory choice was turned off with more inclusive estimates of fertilization success where pre‐ and pericopulatory choice could occur, we show that female mate choice may effectively inhibit sperm competition. Female mate choice and sperm competition (P2) are positively correlated, which is consistent with directional sexual selection in this species. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 67–75.     

Males' evolutionary responses to experimental removal of sexual selection

We evaluated the influence of pre- and post-copulatory sexual selection upon male reproductive traits in a naturally promiscuous species, Drosophila melanogaster. Sexual selection was removed in two replicate populations through enforced monogamous mating with random mate assignment or retained in polyandrous controls. Monogamous mating eliminates all opportunities for mate competition, mate discrimination, sperm competition, cryptic female choice and, hence, sexual conflict. Levels of divergence between lines in sperm production and male fitness traits were quantified after 38-81 generations of selection. Three a priori predictions were tested: (i) male investment in spermatogenesis will be lower in monogamy-line males due to the absence of sperm competition selection, (ii) due to the evolution of increased male benevolence, the fitness of females paired with monogamy-line males will be higher than that of females paired with control-line males, and (iii) monogamy-line males will exhibit decreased competitive reproductive success relative to control-line males. The first two predictions were supported, whereas the third prediction was not. Monogamy males evolved a smaller body size and the size of their testes and the number of sperm within the testes were disproportionately further reduced. In contrast, the fitness of monogamous males (and their mates) was greater when reproducing in a non-competitive context: females mated once with monogamous males produced offspring at a faster rate and produced a greater total number of surviving progeny than did females mated to control males. The results indicate that sexual selection favours the production of increased numbers of sperm in D. melanogaster and that sexual selection favours some male traits conferring a direct cost to the fecundity of females.     

Degree of protandry reflects level of extrapair paternity in migratory songbirds

Males of most migratory organisms, including many birds, precede female conspecifics on their journey to the breeding areas. Several hypotheses have been proposed to explain the evolution of protandrous migration, yet they have rarely been tested at the interspecific level. Here, we provide correlational support for the “mate opportunity” hypothesis, which assumes that selection favours protandry in polygynous species where males gain significant fitness benefits from arriving earlier than females. Drawing on phenological data collected at two northern European stopover sites, we show that the time-lag in spring passage between males and females of five Palearctic migratory songbird species is positively associated with levels of extrapair paternity available from the literature. This suggests that males arrive relatively more in advance of females in species with high sperm competition where sexual selection through female choice is intense. Thus, protandry may arise from selection on the relative arrival timing of males and females rather than from selection within one of the sexes.     

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.     

Extrapair paternity and the evolution of bird song

Bird song is usually considered to have evolved in the contextof sexual selection. Because extrapair paternity is a majorcomponent of sexual selection, mating advantages at the sociallevel for males that produce songs of high quality may be transformedinto higher success in extrapair paternity. Therefore, maleswith longer and more complex songs should suffer less from extrapairpaternity intraspecifically, whereas species with high ratesof extrapair paternity, reflecting intense sperm competition,should produce more elaborate songs. Although some intraspecificstudies demonstrated a negative link between features of songsand extrapair paternity in own nest, others failed to detectsuch a relationship. Contrary to expectation, a meta-analysisof all studies revealed no significant intraspecific evidencefor songs being associated with extrapair paternity. In addition,in comparative analyses based on generalized least squares (GLS)models, we found that no measures of song complexity and temporaloutput were significantly related to extrapair paternity interspecifically,even when potentially confounding factors such as social matingsystem, life history, migration, habitat, or sexual dichromatismwere held constant. Only plumage dichromatism was significantlyrelated to extrapair paternity. The absence of both intra- andinterspecific relationships between measures of song variabilityand extrapair paternity suggests that factors other than postmatingsexual selection have been the important evolutionary forcesshaping differences in song.     

Male-male competition and large size mating advantage in European earwigs, Forficula auricularia

European earwigs are sexually dimorphic in forceps shape and length. Male forceps are thought to be weapons in male contests for access to females, but recent findings suggest that females choose males on the basis of their forceps length. I investigated sexual selection on forceps length and body size and the occurrence of male-male competition. When I controlled for forceps length experimentally and statistically, relatively heavy males had greater copulation success than relatively light males. When I controlled for body size, males with relatively longer forceps had no tendency for greater copulation success than males with shorter forceps. Relatively heavy males more often took over copulations from smaller males than vice versa. Male contests were important for the outcome of mate competition, as males commonly interrupted and took over copulations. My results therefore suggest that intrasexual selection is significant in competition for copulations in male earwigs, and acts on body size. This contrasts with previous findings, which have shown intersexual selection on forceps length to be important. However, both modes of sexual selection may be acting through a two-stage process, where male-male competition first determines which males have access to females, and then through female choice among available males. Morphological measurements supported the conclusion that forceps length and body size are male secondary sexual characters, as these characters had large variance and skewed distributions in males, but were normally distributed in females. Copyright 2000 The Association for the Study of Animal Behaviour.     

Breeding density, cuckoldry risk and copulation behaviour during the fertile period in raptors: a comparative analysis

Extrapair copulations (EPCs) and fertilizations (EPFs) occur in many socially monogamous bird species, including raptors. In this group of species, males invest heavily in reproduction through the feeding of female and young, so the cost of cuckoldry is particularly high. The feeding of females by males, characteristic of most species, conflicts with mate guarding, so raptors are expected to use frequent within-pair copulations (WPCs) for paternity assurance. In this study, I reviewed information on copulation behaviour of diurnal raptors, and used regression analyses and phylogenetic comparative analyses to investigate relations between density, EPC frequency and WPC behaviour. EPCs occurred in most raptor species studied (68%, N=19), mostly during the presumed fertile period of females. EPC frequency, measured as the percentage of females engaging in EPC but not the percentage of extrapair copulations, was positively related to breeding density. The rate and relative duration of WPCs were also positively related to breeding density, but only WPC rate was positively related to EPC frequency (percentage of females). Frequently copulating species had relatively larger testes, underlying higher sperm production capacities. The results support the hypotheses that sperm competition intensity increases with breeding density, and that male raptors rely on frequent copulations to ensure paternity. Despite the risk, EPFs rarely occurred in raptors, suggesting efficient paternity guards.     

Multiple mating and repeated copulations: effects on male reproductive success in red flour beetles

In many insects, both sexes mate multiple times and females use stored sperm for fertilizations. While males frequently engage in two distinct behaviours, multiple mating (with different females) and repeated copulations (with the same female), the reproductive consequences of these behaviours for males have been quantified for only a few species. In this study, males of the red flour beetle, Tribolium castaneum, were found to be capable of mating with as many as seven different virgin females within 15 min. Across sequential copulations with virgin females, there was no decline in either male insemination success or average female progeny production over 48 h. However, when males copulated with previously mated females, there was a significant decline in male paternity success across sequential copulations, possibly due to male sperm depletion. In separate experiments, T. castaneum males were found to engage in two to six repeated copulations with the same, individually marked female. These repeated copulations did not increase male insemination success, short-term female fecundity, or male paternity success. Repeated copulations may possibly play a role in sperm defence. This study indicates that males may frequently engage in multiple matings, but these additional matings may lead to diminishing male reproductive returns.