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.     

Paternity assurance before and after fertilization by male burying beetles (Nicrophorus quadripunctatus)

Parental care requires a large investment of time and energy. This can reduce future parental survival and opportunities for mating. Because males are usually more uncertain of their parentage with respect to the caring of offspring than are females, the reduction in reproductive success is thought to be greater in males. Therefore, males are under selection to ensure paternity of the offspring for which they care. Males can increase paternity before and after fertilization. Before fertilization, males can increase paternity by increasing their competitive ability for fertilization. After fertilization, males can increase paternity by cannibalizing unrelated offspring. Here, we investigated the stage at which male burying beetles, Nicrophorus quadripunctatus, increase their paternity by evaluating the number of offspring sired by a nursing male in asynchronously hatched broods in relation to hatching time. We found that nursing males assure a very high level of the paternity of hatching offspring. We also found that the paternity of non-nursing and nursing males remained constant across hatching time within a brood, indicating that it is unlikely that filial cannibalism plays a role in increasing the paternity of offspring. We concluded that ensuring paternity before fertilization is more important in increasing the paternity of offspring.     

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.     

Factors influencing paternity success in Antechinus agilis: last‐male sperm precedence,timing of mating and genetic compatibility

We describe the patterns of paternity success from laboratory mating experiments conducted in Antechinus agilis, a small size dimorphic carnivorous marsupial (males are larger than females). A previous study found last‐male sperm precedence in this species, but they were unable to sample complete litters, and did not take male size and relatedness into account. We tested whether last‐male sperm precedence regardless of male size still holds for complete litters. We explored the relationship between male mating order, male size, timing of mating and relatedness on paternity success. Females were mated with two males of different size with either the large or the small male first, with 1 day rest between the matings. Matings continued for 6 h. In these controlled conditions male size did not have a strong effect on paternity success, but mating order did. Males mating second sired 69.5% of the offspring. Within first mated males, males that mated closer to ovulation sired more offspring. To a lesser degree, variation appeared also to be caused by differences in genetic compatibility of the female and the male, where high levels of allele‐sharing resulted in lower paternity success.     

Male Mate Choice in the Guppy (Poecilia reticulata): Do Males Prefer Larger Females as Mates?

Although females are the choosier sex in most species, male mate choice is expected to occur under certain conditions. Theoretically, males should prefer larger females as mates in species where female fecundity increases with body size. However, any fecundity‐related benefits accruing to a male that has mated with a large female may be offset by an associated fitness cost of shared paternity if large females are more likely to be multiply mated than smaller females in nature. We tested the above hypothesis and assumption using the Trinidadian guppy (Poecilia reticulata) by behaviourally testing for male mate choice in the laboratory and by ascertaining (with the use of microsatellite DNA genotyping) patterns of male paternity in wild‐caught females. We observed significant positive relationships between female body length and fecundity (brood size) and between body length and level of multiple paternity in the broods of females collected in the Quaré River, Trinidad. In laboratory tests, a preference for the larger of two simultaneously‐presented virgin females was clearly expressed only when males were exposed to the full range of natural stimuli from the females, but not when they were limited to visual stimuli alone. However, as suggested by our multiple paternity data, males that choose to mate with large females may incur a larger potential cost of sperm competition and shared paternity compared with males that mate with smaller females on average. Our results thus suggest that male guppies originating from the Quaré River possess mating preferences for relatively large females, but that such preferences are expressed only when males can accurately assess the mating status of encountered females that differ in body size.     

Genetic parentage assessment in the crayfish Orconectes placidus,a high-fecundity invertebrate with extended maternal brood care

Microsatellite data have recently been introduced in the context of genetic maternity and paternity assignments in high-fecundity fish species with single-parent-tended broods. Here we extend such analyses to an aquatic invertebrate, the crayfish Orconectes placidus, in which gravid females carry large numbers of offspring. Genetic parentage analyses of more than 900 progeny from 15 wild crayfish broods revealed that gravid females were invariably the exclusive dams of the offspring they tended (i.e. there was no allomaternal care), and that most of the females had mated with multiple (usually two) males who contributed sometimes highly skewed numbers of offspring to a brood. Within any multiply sired brood, the unhatched eggs (or the hatched juveniles) from different fathers were randomly distributed across the mother's brood space. All of these genetic findings are discussed in the light of observations on the mating behaviours and reproductive biology of crayfish.     

Breaking the rules: sex roles and genetic mating system of the pheasant coucal

Generally in birds, the classic sex roles of male competition and female choice result in females providing most offspring care while males face uncertain parentage. In less than 5% of species, however, reversed courtship sex roles lead to predominantly male care and low extra-pair paternity. These role-reversed species usually have reversed sexual size dimorphism and polyandry, confirming that sexual selection acts most strongly on the sex with the smaller parental investment and accordingly higher potential reproductive rate. We used parentage analyses and observations from three field seasons to establish the social and genetic mating system of pheasant coucals, Centropus phasianinus, a tropical nesting cuckoo, where males are much smaller than females and provide most parental care. Pheasant coucals are socially monogamous and in this study males produced about 80% of calls in the dawn chorus, implying greater male sexual competition. Despite the substantial male investments, extra-pair paternity was unusually high for a socially monogamous, duetting species. Using two or more mismatches to determine extra-pair parentage, we found that 11 of 59 young (18.6%) in 10 of 21 broods (47.6%) were not sired by their putative father. Male incubation, starting early in the laying sequence, may give the female opportunity and reason to seek these extra-pair copulations. Monogamy, rather than the polyandry and sex-role reversal typical of its congener, C. grillii, may be the result of the large territory size, which could prevent females from monopolising multiple males. The pheasant coucal’s exceptional combination of classic sex-roles and male-biased care for extra-pair young is hard to reconcile with current sexual selection theory, but may represent an intermediate stage in the evolution of polyandry or an evolutionary remnant of polyandry.     

Multiple paternity in a natural population of a wild tobacco fly, Bactrocera cacuminata (Diptera: Tephritidae), assessed by microsatellite DNA markers

Mating frequency has important implications for patterns of sexual selection and sexual conflict and hence for issues such as speciation and the maintenance of genetic diversity. Knowledge of natural mating patterns can also lead to more effective control of pest tephritid species, in which suppression programmes, such as the sterile insect technique (SIT) are employed. Multiple mating by females may compromise the success of SIT. We investigated the level of polyandry and sperm utilization in a Brisbane field population of the tropical fruit fly, Bactrocera cacuminata (Hering), using seven polymorphic microsatellite loci. The offspring of 22 wild-caught gravid females were genotyped to determine the number of males siring each brood and paternity skew, using the programs gerud and scare. Our data showed that 22.7% of females produced offspring sired by at least two males. The mean number of mates per female was 1.72. Paternal contributions of double-sired broods were skewed with the most successful male having sired between 76.9% and 87.5% of the offspring. These results have implications for SIT, because the level of remating we have identified would indicate that wild females could mate with one or more resident fertile males.     

Multiple Paternity in Polyandrous Barn Owls (Tyto alba)

In polyandrous species females produce successive clutches with several males. Female barn owls (Tyto alba) often desert their offspring and mate to produce a 2^nd annual brood with a second male. We tested whether copulating during chick rearing at the 1^st annual brood increases the male''s likelihood to obtain paternity at the 2^nd annual breeding attempt of his female mate in case she deserts their brood to produce a second brood with a different male. Using molecular paternity analyses we found that 2 out of 26 (8%) second annual broods of deserting females contained in total 6 extra-pair young out of 15 nestlings. These young were all sired by the male with whom the female had produced the 1^st annual brood. In contrast, none of the 49 1^st annual breeding attempts (219 offspring) and of the 20 2^nd annual breeding attempts (93 offspring) of non-deserting females contained extra-pair young. We suggest that female desertion can select male counter-strategies to increase paternity and hence individual fitness. Alternatively, females may copulate with the 1^st male to derive genetic benefits, since he is usually of higher quality than the 2^nd male which is commonly a yearling individual.     

Exclusive male care despite extreme female promiscuity and low paternity in a marine snail

Males exhibit striking variation in the degree to which they invest in offspring, from merely provisioning females with sperm, to providing exclusive post-zygotic care. Paternity assurance is often invoked to explain this variation: the greater a male's confidence of paternity, the more he should be willing to provide care. Here, we report a striking exception to expectations based on paternity assurance: despite high levels of female promiscuity, males of a marine snail provide exclusive, and costly, care of offspring. Remarkably, genetic paternity analyses reveal cuckoldry in all broods, with fewer than 25% of offspring being sired by the caring male, although caring males sired proportionally more offspring in a given clutch than any other fathers did individually. This system presents the most extreme example of the coexistence of high levels of female promiscuity, low paternity, and costly male care, and emphasises the still unresolved roles of natural and sexual selection in the evolution of male parental care.     

Yearling male great tits, Parus major, suffer more strongly from cuckoldry than older males

In the majority of socially monogamous bird species, females have offspring sired by males other than their social mate as the result of extra-pair copulations. While it is widely recognised that there is considerable variation in the frequency of extra-pair paternity between species, between populations of a species and between individuals of a population, determinants of this variation are surprisingly difficult to establish. With respect to individual variation within a population, it is an important step to test for male and female correlates of cuckoldry to better understand the patterns as well as the adaptive significance of extra-pair mating behaviour. Here, we analysed patterns of extra-pair paternity in relation to male age, female age and their interaction in the great tit Parus major, a socially monogamous passerine with a moderate frequency of extra-pair paternity. Based on a large sample of 316 genotyped first broods from five successive years, we failed to demonstrate interaction effects of male and female age on both the proportion of extra-pair offspring and the likelihood that at least one extra-pair offspring is present within a brood. However, both the proportion of extra-pair offspring and the likelihood of paternity loss were higher for yearling as compared to older males, while this was not the case for yearling vs. older females. Furthermore, the proportion of extra-pair offspring within a brood decreased with increasing age of the attending male in within-individual analyses. We found a comparable effect also for attending females in within-individual analyses, but only when excluding two individuals with 100% extra-pair paternity. A female (extra-pair) mating preference for older males and/or a limited ability of yearling males to prevent cuckoldry in their broods could explain these age-related patterns of paternity loss. Effect sizes, however, were not particularly large and substantial residual variation within age categories suggests the importance of further yet unidentified determinants of variation in paternity loss in the study population.     

Do Female Red-winged Blackbirds Engage in a Mixed Mating Strategy?

Parentage analyses of broods of nestling red-winged blackbirds (Agelaius phoeniceus) revealed that extra-pair fertilizations (EPFs) accounted for 24% of the offspring. 8% of attempted copulations and 13% of male courtship displays during observations of focal females were by extra-pair males. In addition, mates and non-mates often chased and occasionally made physical contact with females; 34% of those chases in which contact was made were extra-pair chases. Females behaved variably during both within-pair and extra-pair events; females crouched less and resisted more frequently during extra-pair courtship than during within-pair courtship. All extra-pair events, whether natural or induced by male removal, were either resisted or accepted by the female. In 318 focal female-hours of observation during the fertilizable period, no female was ever seen in another male's territory soliciting a copulation. In addition, removal of females' mates resulted in frequent extra-pair courtship and copulation; all of these occurred on the removed male's territory. Some females left their mates' territories on occasion — these forays were nearly always off the study area, no female was ever seen copulating with an extra-pair male while on these forays, and neither the frequency nor the duration of female forays correlated with the frequency of extra-pair fertilizations within broods. There were no associations between extra-pair fertilizations and female age, settlement order, nest order, or clutch size. The number of fledglings produced from a nest was significantly positively associated with the number of sires of the brood. Fewer offspring apparently starved in broods that were multiply sired, yet males did not provide courtship feedings during either within-pair or extra-pair copulations, nor was any paternal care provided to young sired through extra-pair matings. The frequency of infertile eggs was low (< 1%); in those instances of infertile eggs the territory owner sired some young in the same nest or another nest on his territory. Fewer broods were a mixture of within-pair and extra-pair paternity than expected by chance. Clear evidence implicating a mixed strategy on the part of females could not be gathered. Because females behaved variably and because not all costs and benefits to females of extra-pair copulations could be measured, it remains possible that female behavior patterns are either (1) part of a mixed strategy, or (2) part of a strategy minimizing the costs of copulation.     

Small Subordinate Male Advantage in the Zebrafish

Dominance is an important determinant of reproductive success in many species, and size is usually an indicator of dominance status, with larger, dominant individuals physically and physiologically preventing smaller subordinates from mating. However, small size may be advantageous in some mating contexts because enhanced manoeuvrability enables males to get closer to females during mating. Here, we determined the paternity success and testes size of dominant and subordinate male zebrafish (Danio rerio), in pairs that controlled for social status. There was no statistical difference in both body size and testes size between dominant and subordinate males. Dominant males sired significantly more offspring than subordinates, but when subordinates were small, they had a greater share of the paternity than larger subordinates. Small male advantage may be one mechanism by which variation in body size is maintained in this species.     

Allocation of Male Parental Care in Relation to Paternity Within and Among Broods of the Common Yellowthroat (Geothlypis trichas)

The relationship between male parental care and paternity has been investigated in a number of avian species, but in many cases the influences of confounding factors, such as variation in male and territory quality, were not addressed. These sources of variation can be controlled for by making within-male comparisons between successive broods or within-brood comparisons between groups of fledglings in a divided brood. We studied the relationship between male parental care and paternity in the common yellowthroat ( Geothlypis trichas ) at three levels: between groups of fledglings in divided broods, between first and second broods of the same pair, and among all broods in the population. In this study we proposed three hypotheses: first, males in double-brooded pairs should provide relatively more parental care to broods in which they have higher paternity; secondly, after fledging and brood division, males should provide more care to related offspring; and finally, among all broods in the population, paternity should be related positively to male parental care. Brood division occurred in many of the broods studied; however, broods were not divided according to fledgling size or paternity. Furthermore, within divided broods, males fed within-pair and extra-pair fledglings at similar rates. For sequential broods of the same pair, male feeding rates were not associated with differences in paternity between broods. Among all broods in the population, males did not provide relatively less care to broods containing unrelated young. The lack of a relationship between male parental care and paternity suggests that either males cannot assess their paternity or the costs of reducing male parental care outweigh the benefits.     

Evidence of multiple paternity in the bluntnose klipfish, <Emphasis Type="Italic">Clinus cottoides</Emphasis> (Blennioidei: Clinidae: Clinini)

Clinids of the tribe Clinini are viviparous fishes occurring in the temperate waters of southern Africa. Females of the genus Clinus exhibit reproductive traits suggesting multiple paternity. These traits include prolonged gestation periods, matrotrophy and superfetation. We tested the hypothesis that broods of the species C. cottoides are sired by multiple males with the use of microsatellites. We genotyped three broods from known mothers and analysed the relationships within each brood using the software program COLONY, we also used allele counting to find evidence of multiple paternity. Our results revealed that multiple paternity occurred in all three broods analysed; two broods likely had two sires and one brood three sires. One male appear to have fathered offspring with separate females. Our study represents the first molecular analysis of parentage in C. cottoides.     

Female choice for good genes and sex-biased broods in guppies

In a population of guppies Poecilia reticulata females were found to prefer large males and the offspring of these males had a higher survival rate than those sired by smaller males, suggesting that females were selecting their mates on the basis of their good genes. The possibility that females differentially invested in male or female offspring depending on the size or attractiveness of their mate was also investigated, but no relationship was found between a male's attractiveness or body size and the sex ratio of the offspring he sired. However, a strong female-biased sex ratio was detected in the broods and the proportion of males produced decreased with the amount of time that a female was confined with a male. The possible reasons for this are discussed.     

Paternity success and the direction of sexual selection in a field population of a semelparous marsupial,Antechinus agilis

Antechinus agilis is a small sexually size dimorphic marsupial with a brief annual mating period of 2-3 weeks. All males die after this period, and females give birth to up to 10 young. Mating is thought to be promiscuous, however, there is no field data to confirm this. Using microsatellites, we investigated paternity patterns over two seasons in a wild population. Male weight was significantly positively related to the number of females fertilized and with the number of offspring sired, in both years. Furthermore, selection gradients indicated selection for larger males. Both results suggest that size dimorphism in A. agilis can be explained by sexual selection for larger males. The proportion of offspring sired within litters, did not relate to male size. Therefore, larger males are more successful through higher mating access, not through their sperm outcompeting that of smaller males. As expected from their known ranging behaviour, the number of offspring within litters left unassigned to a father did not depend on the grid location of the mother. Female size did not differ between successful reproducing and unsuccessful females. However, females that weaned offspring had larger heads than females that did not wean offspring. Males did not 'prefer' mating with larger females, nor did assortative mating occur. From our results, the mating system of A. agilis is clearly promiscuous. Selection for larger males occurred in both years, even though in one year the operational sex ratio was highly female biased, suggesting that the potential reproductive rate is a better predictor of the direction of sexual selection in A. agilis.     

Parental Sex Differences in Food Allocation to Junior Brood Members as Mediated by Prey Size

Individual offspring within a brood may receive different amounts of provisioning from the male and female parents. Some hypotheses suggest that this bias is the result of an active and adaptive choice by parents. An alternative hypothesis is that feeding biases arise as a result of a constraint of fitting large prey items into small gapes. In an experiment with pied flycatchers, Ficedula hypoleuca , we tested for sex-biased allocation to junior nestlings in asynchronous broods and whether this could be explained by active parental choice or by passive allocation according to prey size and gape size. In both control broods and broods with experimentally increased degree of asynchrony, prey types did not differ between parents but females brought smaller prey than males at younger but not older nestling stages. At younger but not older nestling stages, the majority of feeds to junior nestlings were from females, and the smaller nestlings consumed smaller prey than older siblings. However, there was no evidence of active preference of small nestlings by females as parents did not differ in the tendency to bypass a begging senior nestling in order to feed a junior nestling. Provisioning rates by females were lower than those by males when nestlings were young and we suggest that foraging time constraints caused by the need to brood offspring result in females bringing smaller prey than males. In turn, the larger prey brought by males was more often transferred to larger offspring after the smaller ones failed to swallow it. In such cases, 'preferential' feeding of small nestlings by females may simply be a passive side effect of foraging constraints and gape-size limitations.     

Geographic variation of multiple paternity in the American lobster, Homarus americanus

We studied the frequency of multiple paternity for American lobster (Homarus americanus) at three Canadian sites differing in exploitation rate and mean adult size. The probability of detecting multiple paternity using four microsatellite loci and 100 eggs per female was in excess of 99% under various scenarios of paternal contribution. Overall, 13% of the 108 examined females carried a clutch sired by two or three males. Multiple paternity was observed at the two most exploited sites (11% at Magdalen Islands and 28% at Grand Manan Island), whereas single paternity only was observed at the least exploited site (Anticosti Island). Within populations females with a clutch sired by more than one male tended to be smaller than females with a clutch sired by a single male. Based on these and other findings, we postulate a link between female promiscuity and sperm limitation in the American lobster.