Laying-order effects on sperm numbers and on paternity: comparing three passerine birds with different life histories

In birds, the number of sperm trapped between the perivitelline membranes around the ovum is an estimate of sperm numbers present at the time and place of fertilisation in the female reproductive tract. Sperm numbers may vary among species and between eggs in a clutch and can provide information about sperm utilisation and mechanisms of sperm competition. Here, we describe patterns of variation in sperm numbers through the egg-laying sequence in three passerines in which extra-pair paternity is common, but copulation behaviour differs. Sperm numbers showed no systematic change across the laying sequence in blue tits (Cyanistes caeruleus), but decreased significantly with laying order in bluethroat (Luscinia svecica) and tree swallow (Tachycineta bicolor) clutches. This is consistent with observations that blue tits regularly copulate throughout the laying sequence, while bluethroats stop mate guarding and tree swallows reduce their copulation frequency once the first egg is laid. Nevertheless, cases of a sudden increase in sperm numbers in clutches of bluethroats and tree swallows suggest that successful inseminations also occurred after laying started. In blue tits and bluethroats, sperm numbers were not higher on extra-pair sired eggs than on eggs sired by the social male, suggesting that extra-pair copulations are not timed to the period of peak fertility for each egg. More extra-pair offspring originated from eggs laid early in the sequence in blue tits, while there was no systematic bias in bluethroats. Our results suggest that copulations during the laying sequence are predominantly performed by within-pair males in our study species.     

Adoption or infanticide: options of replacement males in the European starling

The behaviour of a male bird towards a potential mate and her clutch may depend both on his expected paternity and on the likelihood that she will produce a replacement clutch if he commits infanticide. In this study we evaluate the choices made by replacement male European starlings Sturnus vulgaris. By removing males before and during laying, we induced other males, mainly neighbours, to mate with the reproductively active females. When the original male was removed before laying, a new male adopted the subsequent clutch in 14 out of 15 cases. When ten females were widowed during their laying period, replacement males never adopted their clutches. The paternity of replacement males was a function of when they replaced the former male. When replacement occurred more than 3 days before egglaying, the new male fathered nearly all offspring; when it occurred the day before laying, the new male still fathered more than every second young. When the original male was removed during his mate’s laying period, in five out of ten cases a replacement male committed infanticide by throwing out the eggs, but this only occurred in one out of 15 cases when removal took place before laying. The evidence for infanticide actually being committed by the replacement male was circumstantial. Four out of six of the females affected by apparent infanticide produced replacement clutches in which the male presumably had higher paternity than in the original clutch. In all cases, the male adopted the replacement clutch. In five cases when the original male was removed during laying, the neighbours neither adopted the brood nor committed infanticide, although they sometimes were seen courting the widowed female and copulating with her. These cases occurred later during laying than those were males comitted infanticide. The time from infanticide to the laying of the replacement clutch tended to increase as infanticide was committed later in the laying sequence. We conclude that strategies of potential replacement males are influenced by their expected paternity in the current brood and the probability that the female will produce an early replacement clutch. Received: 10 March 1995 / Accepted after revision: 28 October 1995     

Certainty of paternity covaries with paternal care in birds

Summary Male investment in parental care has been hypothesized to be affected or not to be affected by their certainty of paternity, depending on the particular assumptions of theoretical models. We used data on paternal care and extra-pair paternity from 52 bird species to determine whether male parental care was related to certainity of paternity. Paternal care was measured as the relative male contribution to nest building, courtship feeding, incubation, and feeding of nestlings, respectively. Males of avian taxa did not provide less parental care during nest building, courtship feeding and incubation if the frequency of extra-pair paternity was high. However, male participation in feeding of offspring was significantly negatively related to the frequency of extra-pair paternity. This was also the case when the effects of potentially confounding variables such as developmental mode of offspring (which may result in males being freed from parental duties), extent of polygyny (which may result in less paternal care), and the frequency of multiple clutches during one breeding season (which may increase the probability of finding fertile females during the nestling period) were controlled statistically. These results suggest that the extent of paternal care has been affected by certainty of paternity, and that sex roles during the energetically most expensive parts of reproduction have been shaped by sperm competition.     

Offspring recognition and the influence of clutch size on nest fostering among male sand gobies, Pomatoschistus minutus

When parental care is costly, parents should avoid caring for unrelated young. Therefore, it is an advantage to discriminate between related and unrelated offspring so that parents can make informed decisions about parental care. In the present study, we test the hypothesis that male sand gobies (Pomatoschistus minutus) recognize and differentially care for their own offspring when given a choice between a nest with sired eggs and a second nest with eggs sired by an unrelated male. The sand goby is a species with exclusive and costly paternal care. Male parasitic spawnings (e.g., sneaking) as well as nest takeovers by other males are common. Our results show that nests containing sired eggs were preferred and received significantly more care, as measured by nest building and nest occupancy, than nests with foreign eggs even when males cared for both nests. These findings suggest that males respond to paternity cues and recognize their own clutches. Relative clutch size also had a significant effect on male parental care. When sired clutches were larger than foreign clutches, males preferred to care for their own nest. In the few cases where males chose to take care of foreign nests, the foreign clutch was larger than their own clutch. Taken together, our results provide evidence that both paternity cues and clutch size influence parenting decisions among male sand gobies.     

Mate guarding,copulation strategies and paternity in the sex-role reversed,socially polyandrous red-necked phalarope<Emphasis Type="Italic"> Phalaropus lobatus</Emphasis>

In a recent review, Westneat and Stewart (2003) compiled evidence that extra-pair paternity results from a three-player interaction in which sexual conflict is a potent force. Sequentially polyandrous species of birds appear to fit this idea well. Earlier breeding males may attempt to use sperm storage by females to obtain paternity in their mates subsequent clutches. Later-breeding males may consequently attempt to avoid sperm competition by preferring to pair with previously unmated females. Females may bias events one way or the other. We examined the applicability of these hypotheses by studying mating behavior and paternity in red-necked phalaropes (Phalaropus lobatus), a sex-role reversed, socially polyandrous shorebird. Male red-necked phalaropes guarded mates more strongly than other shorebirds. Males increased within-pair copulation attempts during their mates fertile period, and maintained or further increased attempts towards the end of laying, suggesting an attempt to fertilize the females next clutch; these attempts were usually thwarted by the female. Paired males sought extra-pair copulations with females about to re-enter the breeding pool. Multilocus DNA fingerprinting showed that 6% of clutches (4/63) each contained one chick sired by a male other than the incubator, producing a population rate of these events of 1.7% (n=226 chicks). Male mates had full paternity in all first clutches (n=25) and 15 of 16 monogamous replacement clutches. In contrast, 3 of 6 clutches of second males contained extra-pair young likely fathered by the females previous mate. Previously mated female phalaropes may employ counter-strategies that prevent later mating males from discriminating against them. The stability of this polyandrous system, in which males provide all parental care, ultimately may depend on females providing males with eggs containing primarily genes of the incubating male, and not a previous mate.Communicated by M. Webster     

Is female promiscuity constrained by the presence of her social mate? An experiment with bluethroats <Emphasis Type="Italic">Luscinia svecica</Emphasis>

Extra-pair paternity is common in birds and much research has focussed on the selective advantage of extra-pair matings for both sexes. In contrast, little attention has been given to the fact that in most species the majority of offspring are sired by the social male. We investigated whether extra-pair matings of female bluethroats (Luscinia svecica) are constrained by the presence of the pair male, by detaining males in cages on their territories for one morning during the peak of female fertility. The proportion of offspring sired by extra-pair males was higher in broods where males had been detained (35%) than in control broods (16%), while the proportion of broods that had at least one extra-pair offspring did not differ significantly between experimental (65%) and control broods (44%). Within the experimental group, levels of extra-pair paternity were not related to the day of experiment in relation to start of egg laying, but males caught early in the morning lost more paternity than males caught later on. Our results show that pair males exert constraints on the frequency of extra-pair paternity by being present during the period of peak fertility, which could be a direct effect of their mate guarding effort and/or due to an advantage in sperm competition for pair males.     

Time and recruitment costs as currencies in manipulation studies on the costs of reproduction

Life history theory predicts that parents will have lower Darwinian fitness if they tend clutches that are above or below the size they naturally produce. We experimentally tested for relationships between fitness and clutch size in Tree Swallow (Tachycineta bicolor) offspring and parents. Over 130 trios of nests initiated on the same day were randomly divided among reduce (-3 eggs), control (3 eggs picked up and replaced), or add (+3 eggs) manipulations. Pre-manipulation modal clutch size was six eggs (range before manipulations was 1-10; afterwards, it was 1-11). Hatching took longer in larger clutches, but the proportion of eggs hatching and fledging was similar for clutches from 4 to 10, so that clutches of 10 produced the maximum number of fledgling. Parental feeding rates were higher for larger broods, but per capita feeds to nestlings were fewer, and nestlings were smaller. Nonetheless, survival of both young and adults, based on recaptures in subsequent years, was not significantly affected by manipulations. Manipulations also had no significant effect on subsequent reproduction, including the number of fledglings produced by either local recruits or returning breeders. Collectively, our results failed to detect fitness costs associated with tending larger clutches for either parents or the offspring reared and suggested directional selection for larger clutch size. However, because clutches that hatch later produce fewer recruits, the extra days required to lay more eggs and to fledge extra young may eliminate a large part of the advantage that would accrue to parents producing enlarged clutches. For example, our data suggest that there may be less than a 16% benefit to producing nine instead of six eggs, rather than 50%, as is suggested by experimentally manipulated egg numbers alone. Thus, time, rather than costs of reproduction, may be the crucial constraint selecting against Tree Swallows laying larger clutches.     

Female control of extra-pair fertilization in tree swallows

Summary In a Canadian population of tree swallows, Tachycineta bicolor, DNA fingerprinting has previously shown that half of all broods contain many offspring resulting from extra-pair copulations (EPCs), whereas the other half contain only legitimate offspring. This bimodal pattern of extra-pair paternity might be due to variation in the effectiveness of male paternity guards, variation in female ability to resist EPCs, and/or variation in female pursuit of EPCs. Here we report experimental evidence for female control of copulations and fertilizations and the occurrence of two alternative copulation strategies among females in this population. Ten paired male tree swallows were removed on the day their mates laid the first egg. Replacement males took over the nestbox within 0.5–23 h and attempted to copulate with the widowed female. Assuming that eggs were fertilized approximately 24 h prior to laying, the first two eggs were fertilized before the male was removed, while the third and subsequent eggs could potentially be fertilized by the replacement male. Fingerprinting revealed that the first two eggs were sired by the resident males in five nests and by extra-pair males in the remaining five nests. The widows that had been faithful to their initially chosen mate rejected copulation attempts by the replacement male until most of the eggs had been laid. Consequently, nearly all eggs laid by these females were sired by the original male. The widows that had been unfaithful prior to male removal copulated sooner with the replacement male than females that were faithful to their mate. However, these replacement males also had a very low fertilization success; most eggs were sired by males that were not associated with the nest. This is consistent with the situation in non-experimental nests where unfaithful females copulate with their mate at the same rate as faithful females, yet unfaithful females have a majority of offspring sired by extra-pair males. We conclude that fertilization patterns to a large extent are determined by the female through active selection and rejection of copulation partners, though our results also allow some speculation that females have control over sperm competition. Female copulation tactics are probably determined some currently unknown fitness benefits of having the offspring sired by particular males.Correspondence to: Raleigh J. Robertson     

Multiple paternity, sperm storage, and reproductive success of female and male painted turtles (Chrysemys picta) in nature

When females receive no direct benefits from multiple matings, concurrent multiple paternity is often explained by indirect genetic benefits to offspring. To examine such possibilities, we analyzed genetic paternity for 1,272 hatchlings, representing 227 clutches, from a nesting population of painted turtles (Chrysemys picta) on the Mississippi River. Goals were to quantify the incidence and distribution of concurrent multiple paternity across clutches, examine temporal patterns of sperm storage by females, and deduce the extent to which indirect benefits result from polyandrous female behaviors. Blood samples from adult males also allowed us to genetically identify the sires of surveyed clutches and to assess phenotypic variation associated with male fitness. From the genetic data, female and male reproductive success were deduced and then interpreted together with field data to evaluate possible effects of female mating behaviors and sire identity on offspring fitness. We document that more than 30% of the clutches were likely fathered by multiple males, and that presence of multiple paternity was positively correlated with clutch size. Furthermore, the data indicate that the second male to mate typically had high paternity precedence over the first.     

Paternity analysis of two male mating tactics in the fiddler crab, Uca mjoebergi

The fiddler crab Uca mjoebergi mates both underground in male-defended burrows and on the surface near female-defended burrows. The reproductive tract of Uca species facilitates last-male precedence, suggesting that males that do not guard-mated females are likely to gain very little paternity if the female re-mates with another male. Here, we test the reproductive success of burrow and surface matings using paternity analysis. We found that 100?% of the females that mated in burrows extruded a clutch of eggs. Furthermore, we show conclusively, for the first time in a fiddler crab species, that last-male sperm precedence results in the majority of the female’s eggs being fertilised by the burrow-mated male. In contrast, surface matings resulted in significantly fewer females extruding eggs (5.6?%). Paternity analysis also revealed that more than half of the clutches from burrow-mated females showed low levels of extra-pair paternity from previous matings. Although multiple matings appear common in U. mjoebergi, burrow-mated males that guard females are guaranteed a successful mating with extremely high rates of assured paternity. Surface matings therefore appear to be an opportunistic tactic that may increase male reproductive success in a highly competitive environment.     

Genetic relationship between offspring and guardian adults of a rhacophorid frog and its care effort in response to paternal share

The rhacophorid frog, Kurixalus eiffingeri, is one of only a few frog species that exhibits polyandry and paternal care of eggs. Previous studies predicted that multiple paternity within an egg clutch could influence the degree of paternal care and reproductive strategies. We used microsatellite DNA markers to assess the prevalence of multiple paternity within egg clutches and the relationship between male paternal care and the percent of male’s genetic contribution to the clutch, i.e., paternal share. We conducted field observations of paternal care and collected tissues from both male frogs and tadpoles for parentage analyses. Our results showed that at least five out of 31 egg clutches had multiple paternity. Attending males were always the genetic fathers of some, if not all of the eggs in the clutch they guarded. All egg clutches except one were attended by one male frog but the attending male did not necessarily sire the majority of offspring. Multiple paternity in all cases consisted of two fathers and one mother and most likely resulted from synchronous polyandry. Paternal care effort correlated significantly with the male’s genetic contribution to the clutch, suggesting that male frogs adjust the effort expended in care in response to paternal share. In addition, our results suggest that externally fertilizing species with parental care and multiple paternity may develop novel reproductive and behavioral strategies to safeguard their parental investment and overcome sperm competition.     

Extra-pair paternity and tail ornamentation in the barn swallow Hirundo rustica

Females of socially monogamous species may copulate with attractive non-mates to obtain access to the genes of such males, and a preference for attractive copulation partners may result in sexual selection. Extra-pair copulations are common in the socially monogamous barn swallow Hirundorustica, and a 2-year study of paternity using multi-locus DNA fingerprinting demonstrated that 33% of 63 broods and 28% of 261 offspring were sired by extra-pair males. The frequency of extra-pair offspring within broods was highly skewed with the majority of all broods having either no extra-pair offspring or only extra-pair offspring. Individual pairs were consistent in their frequency of extra-pair paternity among broods, and the repeatability of extra-pair paternity of multiple broods of the same female was statistically significant. The proportion of extra-pair offspring was negatively related to the tail length of the male attending the nest. Behavioural observations showed that extra-pair fertilizations were more likely in broods raised by females that had been observed to engage in extra-pair copulations. The frequency of extra-pair offspring was unrelated to the intensity of two male paternity guards, mate guarding and the rate of intra-pair copulations. In an analysis of extra-pair paternity and male parental care in different broods of the same male, male barn swallows fed their offspring relatively less frequently if the brood contained more extra-pair offspring. Therefore, female barn swallows pursue extra-pair copulations with attractive males, which may result in sexual selection, even though extra-pair paternity is costly for females due to the reduction of paternal care by their social mates. Received: 24 January 1997 / Accepted after revision: 2 August 1997     

Current versus future reproduction: an experimental test of parental investment decisions using nest desertion by mallards (<Emphasis Type="Italic">Anas platyrhynchos</Emphasis>)

Past investment in offspring may be important in determining a parent's ability to reproduce in the future and, hence, should affect the relative value of current offspring. However, there have been surprisingly few clear tests of whether animals actually adjust parental care in response to diminished opportunities for future reproduction. We modified the experimental protocol of Sargent and Gross [Behav Ecol Sociobiol (1985) 17:43–45] to examine offspring desertion by mallards ( Anas platyrhynchos), and decoupled the influence of past investment from expected current benefits by controlling for the effect of offspring age on clutch value. Using 9 years of nest mortality data, we accounted for the increasing prospects of egg survival with clutch age by calculating clutch sizes throughout incubation with equivalent expected benefits. Applying this approach, we experimentally reduced 203 clutches at two different incubation stages such that they had equivalent expected benefits but differed in the amount of past investment. Nest desertion rates did not differ between early- and late-incubated clutches that had equivalent expected benefits. Rather, the probability of desertion increased with the severity of the clutch reduction treatment. These results suggest that female mallards adjust parental care according to the expected benefits of current offspring, rather than to diminished prospects for future reproduction due to past investment. We further examined whether females assessed expected benefits on the basis of clutch size alone or clutch size adjusted for the age of the clutch. Using Akaike's Information Criterion, the most parsimonious model to explain the probability of deserting an experimentally reduced clutch included both the proportion of the clutch remaining and clutch age. Thus, female mallards appear to fine-tune their level of parental care not only according to the relative number of offspring in the clutch, but also to the increased prospects for offspring survival as they age.     

Maternal effects on begging behaviour: an experimental demonstration of the effects of laying sequence, hatch order, nestling sex and brood size

Differential resource allocation by females across the laying sequence has been hypothesised as a mechanism through which females could either compensate nestlings that hatch last in asynchronous broods or promote brood reduction. In this study we artificially incubated eggs and cross-fostered offspring to manipulate nestlings’ position in the hatching order, to identify whether the competitive ability of nestlings is dependent on position in the laying sequence. In both control and experimentally reversed broods, first hatched chicks had a higher survival than last hatched siblings. Yet, nestlings that hatched from eggs laid in the second half of a clutch begged with a greater intensity than nestlings hatched from eggs laid in the first half of a clutch. In natural broods, the greater begging competitiveness of nestlings from later-laid eggs led to a moderation of sibling competition and these nestlings achieved the same body size and weight as nestlings from eggs laid in the first half of the clutch. The lack of a substantial difference in the size and condition of surviving nestlings in respect to laying order suggests that differential resource allocation across the egg-laying sequence partially compensates for hatching last in asynchronous broods and reduces the negative effects of the nestling size hierarchy. The effect of laying order, brood size and experimental treatment also differed for male and female nestlings. Our study highlights the need to be aware of the complex and subtle effects of nestling sex and laying sequence when investigating genetic and environmental influences on individual fitness.     

Female sand gobies gain direct benefits by choosing males with eggs in their nests

In some fish species with paternal care, females prefer to spawn with males whose nests already contain eggs. Several hypotheses have been put forward to explain this behaviour, such as reduced risk of predation or cannibalism (the dilution effect), increased parental investment, and mate copying. This experimental study focuses on female mate choice in the sand goby, Pomatoschistus minutus. Females were found to choose males with eggs in their nests. In addition, hatching success increased with clutch size, mainly because males with larger clutches showed less filial cannibalism. Increased egg survival in large clutches may thus be explained by a combination of the dilution effect and higher parental investment. In another experiment, females did not seem to copy the observed mate choice of other females. In conclusion, female preference for males with eggs in their nests is adaptive, and can be explained by direct benefits, as more surviving offspring are produced. Received: 23 December 1995/Accepted after revision: 11 May 1996     

Extra-pair paternity and intraspecific brood parasitism in wild zebra finches Taeniopygia guttata,revealed by DNA fingerprinting

Summary The frequency of extra-pair parentage in a wild population of zebra finches Taeniopygia guttata was examined by DNA fingerprinting. A total of 25 families, comprising 16 pairs of parents and 92 offspring (in broods of 1 to 6) were examined. Ten cases of extra-pair parentage, presumed to constitute intraspecific brood parasitism, were detected (10.9% of offspring or 36% of broods), including one possible instance of quasi-parasitism (parasitism by a female fertilized by the male nest owner). The average number of parasitic eggs per clutch detected by fingerprinting was 1.10±0.32 SD, very similar to the one egg difference in average clutch size between parasitised (6.0±0.82) and unparasitised nests (5.0±0.95). Two cases of extra-pair paternity (EPP) were detected among 82 offspring whose maternity was confirmed: 2.4% of offspring, or 8% of broods. In both cases EPP accounted for only a single offspring within a brood. Behavioural observations show that EPP occurs through extra-pair copulation rather than rapid mate switching. The results are discussed in the light of what is known about the fertile period and sperm precedence patterns in this species. Offprint requests to: T.R. Birkhead     

Social and ecological factors affecting paternity allocation in American robins with overlapping broods

Factors that affect extra-pair mating in birds are likely to vary across the breeding season. Changing densities of active nests may alter the opportunities for extra-pair mating, and parental duties may alter a male’s opportunity to guard his mate from extra-pair mating. The latter affects species with multiple broods, where males care for fledglings from first nests while females initiate second nests. We studied a population of multi-brooded American robins (Turdus migratorius) to assess how seasonal changes in nesting density and changes in mate-guarding opportunity influenced paternity patterns over successive breeding attempts. Extra-pair paternity (EPP) occurred in 71.9% of broods and accounted for 48.1% of young. High nesting densities in the study population may explain the high overall rate of EPP, but seasonal variation in breeding density did not explain patterns of EPP among nests. Contrary to the predictions of the mate-guarding hypothesis, EPP did not increase in the second nests that followed successful first nests, and the percentage of extra-pair young in second nests did not decline as the overlap between successive nests increased. The fact that EPP was actually lower when the interval between clutches was shorter suggests that the sooner the males can assume sole care of first broods and allow their mates to renest (indicative of superior paternal quality), the more paternity they realize in the next nest. These results suggest that mate-guarding opportunity does not influence paternity in this population of American robins and that female robins may allocate paternity based on their assessment of male parental performance at first nests.     

An adaptive annual rhythm in the sex of first pigeon eggs

When the reproductive value of male and female offspring varies differentially, parents are predicted to adjust the sex ratio of their offspring to maximize their fitness (Trivers and Willard, Science 179:90–92, 1973). Two factors have been repeatedly linked to skews in avian offspring sex ratio. First, laying date can affect offspring sex ratio when the sexes differ in age of first reproduction, such that the more slowly maturing sex is overproduced early in the season. Second, position of the egg in the laying sequence of a clutch may affect sex ratio bias since manipulating the sex of the first eggs may be least costly to the mother. We studied both factors in two non-domesticated pigeon species. Both the Wood pigeon (Columba palumbus) and the Rock pigeon (Columba livia) have long breeding seasons and lay two-egg clutches. In the field, we determined the sex of Wood pigeon nestlings. In Rock pigeons, housed in captivity outdoors, we determined embryo sex after 3 days of incubation. On the basis of their sex-specific age of first reproduction, we predicted that males, maturing at older age than females, should be produced in majority early and females later in the year. This was confirmed for both species. The bias was restricted to first eggs. Rock pigeons produced clutches throughout the year and show that the sex of the first egg followed an annual cycle. To our knowledge, this study presents the first evidence of a full annual rhythm in adaptive sex allocation in birds. We suggest that this reflects an endogenous seasonal program in primary sex ratio controlled by a preovulatory mechanism.     

Long-lasting consequences of elevated yolk testosterone levels on female reproduction

Maternal yolk androgens in bird eggs represent an important pathway along which offspring phenotype is shaped. Most of the hormone-mediated maternal effects are highly important in the context of sibling competition. However, there is also increasing evidence for long-lasting effects far beyond the nestling period, and these effects may have important consequences on the reproductive success of the offspring. Here, we investigated the effects of experimentally elevated yolk testosterone concentrations on growth and reproduction in female canaries. Elevated yolk testosterone concentrations enhanced the post-natal growth rate, but not the asymptotic mass, and reduced the survival probability. The latter may be a consequence of the higher growth rate, which may have rendered females hatching from testosterone-treated eggs (T-females) more vulnerable to harsh environmental conditions. Adult T-females made a larger investment in their clutch by laying more but not heavier eggs than females hatching from control-treated eggs. Our results suggest that the observed long-lasting effect on clutch size relates to changes in the growth trajectory rather than being a direct consequence of testosterone, since studies manipulating early growth conditions obtained similar results. Clearly, further studies are now required in order to investigate the intriguing relationship between yolk testosterone, elevated growth rates, and clutch size.     

Sperm storage reflects within- and extra-pair mating opportunities in a cooperatively breeding bird

In passerine birds, storage and maturation of sperm takes place in the cloacal protuberance (CP), an external swelling of the reproductive organ. The considerable variation in CP size among species is presumed to be a consequence of varying levels of sperm-competition, but whether individual variation in CP size within a species also reflects sperm competition is not well established. Here, we study temporal variation in male CP size in relation to within-pair and extra-pair mating opportunities and cuckoldry risk in purple-crowned fairy-wrens Malurus coronatus. This is a socially monogamous cooperatively breeding passerine that can breed year-round and has low levels of extra-pair paternity (in 6?% of broods). We show that male CP size sharply increased a few weeks before, and rapidly regressed after his partner laid eggs, consistent with a cost of its maintenance and/or sperm production. Surprisingly, despite low levels of extra-pair paternity, CP size of non-breeding and pre-breeding males was positively correlated with the number of breeding females in the population, suggesting that CP size is sensitive to extra-pair mating opportunities. However, CP sizes do not seem to reflect cuckoldry risk: CP size of dominant males was unaffected by the presence of a subordinate that was unrelated to the dominant female, although those subordinates occasionally sire offspring, and had a larger CP than subordinates living with their mother. Our results suggest that, even in a species with low levels of extra-pair paternity, individual investment in sperm storage reflects both within-pair and, albeit to lesser extent, extra-pair mating opportunities.