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.     

Male spottail darters (Etheostoma squamiceps) do not use chemical or positional cues to discriminate between sired and foster eggs

Filial cannibalism is hypothesized to allow nest-guarding males to recoup energy lost during nest defense. Males in many species of fishes occasionally defend broods containing both sired and foster eggs due to shifts in nest site ownership or cuckoldry. Such males are predicted to consume primarily foster eggs if the ability to discriminate among eggs exists. In a previous laboratory study, male spottail darters (Etheostoma squamiceps) consumed significantly more foster eggs than sired eggs, suggesting the existence of a mechanism for discrimination using chemical or positional cues. This discrimination mechanism in the spottail darter was tested by creating nest sites with half sired eggs and half foster eggs (n=15), or with all sired eggs with half positionally relocated (n=9). Males defended these nests for 2 days in the field, and cannibalism was determined by counting eggs lost during that interval. Neither foster eggs nor relocated sired eggs were consumed in greater numbers or percentages of the original brood sizes than the unchanged sired eggs, indicating that male spottail darters do not discriminate between foster and sired eggs by olfaction or position. Alternatively, the hypothesis that males treat all eggs in nest sites in which they have spawned as sired explains the results of both studies.     

Cannibalize or care? The role of perceived paternity in the sand goby, <Emphasis Type="Italic">Pomatoschistus minutus</Emphasis>

Parental care is a costly part of reproduction. Hence, natural selection should favor males which avoid caring for unrelated young. However, the decision to abandon or reduce care requires cues which are evaluated to give information on potential reproductive value of the offspring. The prediction that male sand gobies, Pomatoschistus minutus, care for foreign eggs as long as they were spawned in their own nest and at least some of such cues are fulfilled was tested. Egg-guarding males that had recently taken part in a spawning event were given a clutch of eggs that was sired either by themselves or another male, in either their own or another male’s aquarium. Males that had not taken part in a spawning event were used as controls and were given eggs sired by another male. We measured the amount of filial cannibalism and nest building. Control group males did not care for eggs and ate them all before rebuilding the nest. In the other treatments, there were no significant effects of paternity, though males moved to another male’s aquarium increased their clutch area threshold and completely consumed larger clutches than males that were not moved. There was no intermediate response in any treatment in the form of increased partial filial cannibalism or less well-constructed nests. Our results suggest that egg-guarding males cannot distinguish between eggs sired by themselves and those sired by other males but are able to react to cues indicating paternity state. Males do not adopt eggs to attract females in P. minutus.     

Paternal care and egg survival both increase with clutch size in the fathead minnow,Pimephales promelas

Summary In some species of fishes with paternal care, females prefer to spawn with males who are already defeding eggs; moreover, in many species, paternal care increases with the number of eggs that a male is defending. If egg survival depends on the level of paternal care, and is largely independent of egg number, then egg survival should increase with clutch size. This result would provide a potential adaptive mechanism for female preference for males with eggs. I examined the effects of clutch size on paternal care and egg survival in the fathead minnow, Pimephales promelas, and found that both increased with male clutch size.     

Paternity and paternal care in the polygynandrous Smith's longspur

In species where females copulate with more than one male during a single breeding attempt, males risk investing in offspring that are not their own. In the polygynandrous Smith's longspur (Calcarius pictus), females copulate sequentially with one to three males for each clutch of eggs and most of these males later assist in feeding the young. Using multilocus DNA profiling, we determined that there was mixed paternity in >75% of broods (n=31) but that few offspring (<1% of 114 nestlings) were sired by males outside the polygynandrous group. Male feeding rate increased significantly with the number of young sired, with males siring four nestlings feeding the brood at double the frequency of males siring only a single nestling. However, male Smith's longspurs appear to show a graded adjustment of paternal care in response to paternity only when other males are available to compensate for reduced care: feeding rate did not vary in relation to paternity when only one male provisioned young at the nest. There was no evidence that males could recognise their own offspring within a brood and feed them preferentially. The number of offspring sired by each male was significantly correlated with the number of days spent copulating with the attending female: on average, a male sired one offspring for every 2 days of copulatory access. If males use their access to females to estimate paternity (and thereby decide on their subsequent level of parental investment), a positive relationship is expected between the amount of female access and the subsequent feeding rate to the nestlings. Nonetheless, male feeding effort was only weakly correlated with female access and more study is needed to determine how males estimate their paternity in a brood. Received: 1 June 1997 / Accepted after revision: 1 April 1998     

Sexual selection in a socially monogamous bird: male color predicts paternity success in the mountain bluebird, <Emphasis Type="Italic">Sialia currucoides</Emphasis>

Ornamental traits are thought to evolve because they give individuals an advantage in securing multiple mates. Thus, the presence of ornamentation among males in many monogamous bird species presents something of a conundrum. Under certain conditions, extra-pair paternity can increase the variance in reproductive success among males, thus increasing the potential for sexual selection to act. We addressed this possibility in the mountain bluebird (Sialia currucoides), a socially monogamous songbird in which males possess brilliant ultraviolet (UV)-blue plumage. Specifically, we asked whether a male’s success at siring offspring within his own nest and within the nests of other males was related to his coloration. In pairwise comparisons, males that sired extra-pair offspring were not more colorful than the males that they cuckolded. However, males that sired at least one extra-pair offspring were, on average, brighter and more UV-blue than males that did not sire extra-pair offspring. Brighter, more UV-blue males sired more offspring both with their own mate and tended to sire more offspring with extra-pair mates and thus sired more offspring overall. Our results support the hypothesis that the brilliant UV-blue ornamental plumage of male mountain bluebirds evolved at least in part because it provides males with an advantage in fertilizing the eggs of multiple females.     

The costs of male parental care and its evolution in a neotropical frog

Summary Parental care is practiced exclusively by males of the Puerto Rican frog, Eleutherodactylus coqui. Males brood clutches of direct-developing eggs in non-aquatic nest sites and defend eggs against cannibalistic nest intruders. Here, I report on energetic and mating costs incurred by males that provide parental care, and suggest how these proximate costs affect male fitness and the evolution of male parental care in this species. Energetic costs are small for brooding males in comparison to non-brooding, calling males. Brooding males had a higher frequency of empty stomachs and lost small, but significant, fractions of their initial body mass during parental care. Abdominal fat bodies of brooding males during the middle third of parental care were significantly smaller than those of calling males; those of males brooding eggs in earlier or later stages were not different. The mating cost of parental care is greater. Most brooding males cease calling during parental care. However, gravid females are available (i.e., known to mate) on most nights during the principal breeding season; hence non-calling males miss potential opportunities to mate. A mating cost was estimated by calculating nightly mating probabilities for calling males in a plot where nightly calling male densities and daily oviposition schedules were known. On average, a male exhibiting normal calling behavior would be expected to obtain a new mate once every 35.7 days. Hence a brooding male that ceased calling for a 20-day parental care period would miss, on average, 0.56 additional mates. Males that were more successful than average in attracting mates could miss up to 1.63 matings. A marginal value model (Fig. 1) is used to analyze the net effect on male fitness of parental care benefits and costs in E. coqui (Fig. 3). The model indicates that males garner the highest reproductive success by providing care from oviposition through hatching. There is no stage during the pre-hatching period at which a desertion strategy would yield higher reproductive success. In fact, the model suggests that males should provide full parental care even in the face of much higher mating costs than currently obtain in the system.     

Brood defense and filial cannibalism in the spottail darter (<Emphasis Type="Italic">Etheostoma squamiceps)</Emphasis>: the effects of parental status and prior experience

Male spottail darters (Etheostoma squamiceps) defend nest sites in which females deposit eggs over the course of several weeks. In laboratory experiments, I tested three predictions of the hypothesis that the presence of eggs increases the value of a nest site to male spottail darters: (1) males should preferentially defend nests with eggs over empty nests, and males that sired the eggs should (2) spend more time defending them and (3) consume less of their broods than should alloparent males. Parent males were tested using eggs they were guarding in the field; alloparents included males that were not defending eggs immediately prior to the experiment (inexperienced), and males that were defending eggs in the field when captured but were given eggs sired by a different male (experienced). In choice experiments in which males were offered nest sites differing only in the presence of eggs, males preferred to defend nest sites with eggs regardless of parental status. Parent males spent significantly more time defending eggs and consumed less of their broods than did inexperienced alloparent males. Experienced alloparent males were similar to parent males in brood defense but had levels of filial cannibalism similar to inexperienced males, suggesting that prior experience may influence brood defense but not egg consumption.     

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     

Allopaternal care in the fathead minnow,Pimephales promelas: females prefer males with eggs

Summary Some species of fishes with exclusive male parental care exhibit the phenomenon of allopaternal care; that is, some males acquire and care for other males' eggs. We conducted a series of experiments to investigate the dynamics and evolution of allopaternal care in one such species, the fathead minnow (Pimephales promelas). In choosing a nest site, a newly reproductive male tended to take over the nest site of a parental male by evicting the resident male, rather than occupy a physically identical empty nest site. The new male generally cared for the old male's eggs, and in most cases, daily egg survival improved under the new male's care. When males were given a choice among unguarded nest sites, they preferred to occupy nest sites already containing eggs. When eggs were randomly assigned to nesting males, females preferred to spawn with males who had eggs in their nest sites. Thus, it appears that female preference for males with eggs led to the evolution of allopaternal care in the fathead minnow.     

Yolk androgen deposition as a compensatory strategy

The deposition of androgens into the yolks of eggs can have long-lasting effects on the growth and development of young birds. It has been proposed that female birds and reptiles deposit yolk androgens according to the differential allocation hypothesis (DAH), which posits the allocation of more resources to offspring sired by more attractive, higher-quality males. We examined deposition patterns of yolk androgens in relation to mate attractiveness in the house finch Carpodacus mexicanus. Contrary to the predictions of the DAH, female house finches deposited significantly more androgens into eggs sired by less attractive males. We propose that, rather than serving as resources, androgens are used as mediators in a compensatory distribution strategy, enabling females to improve the quality of young produced with less attractive males.     

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.     

Egg-mimicry as a mating strategy in the fantail darter,Etheostoma flabellare: females prefer males with eggs

Summary In some species of fishes with paternal care, females prefer to spawn with males already defending eggs. Such female preference appears to have resulted in adoption of unrelated eggs as a male mating strategy in several species. Page and Swofford (1984) proposed that such female preference may have also resulted in the evolution of male egg-mimics in several species of darters (Percidae); however, their hypothesis has not been tested. We examined female preference in the fantail darter (Etheostoma flabellare) and found that females preferred males with eggs over males without eggs, and males with egg-mimics over males without egg-mimics. Thus it appears that female preference for males already guarding eggs may have led to the evolution of specialized egg-mimicking morphology in males.     

Alternative male mating tactics in a cichlid, Pelvicachromis pulcher: a comparison of reproductive effort and success

Pelvicachromis pulcher is a small African cichlid which breeds in holes. Males may either reproduce monogamously (pair males), polygynously (harem males), or be tolerated as helpers in a harem territory (satellite males). These helpers share in defence of the territory against conspecifics, heterospecific competitors and predators. There are two male colour morphs that are fixed for life and are apparently genetically determined. These differ in their potential mating strategy. Red morph males may become harem owners, while yellow morph males may become satellite males, and males of both morphs may alternatively pair up monogamously. We compared the reproductive effort and success of these three male reproductive strategies. Effort was measured as attack rates, time expenditure and the risk of being injured or killed when attacking competitors or predators of three sympatric fish species. Reproductive success was measured by observing how many eggs were fertilized by each male when this was possible, and by using genetic markers. The number of fry surviving to independence of parental care was used as a criterion of success. The reproductive success of harem males was 3.3 times higher than that of pair males and 7 times higher than that of the average satellite male. Dominant satellite males, however, were as successful as monogamous pair males, using the measure of fertilized eggs. To our knowledge, this has not been found previously in any fish species. Both harem and pair males had lower parental defence costs per sired offspring, however, than males using the alternative satellite tactic. Defence effort was significantly related to the risk of injury. Received: 17 January 1996 / Accepted after revision: 9 June 1997     

Effects of costs and benefits of brood care on filial cannibalism in the sand goby

This study tested experimentally whether clutch size and the cost of care affect filial cannibalism in the sand goby, Pomatoschistus minutus. Evolutionary models of filial cannibalism suggest that egg eating has evolved as a way for the male parent to prolong his breeding season. These models assume that eggs function as an alternative energy source for the constrained parent. I manipulated clutch size by allowing males to mate with either one or two females, representing a small and a large clutch, respectively. The addition of a small male shore crab, a common egg predator, increased the cost of care. I quantified fat reserves as a measure of the condition of guarding males. Males who did not build nests had lower fat reserves than males who built nests, suggesting that males with low energy reserves do not start breeding. Males with small clutches lost their nest to the crab more often than males with large clutches. Neither filial cannibalism nor the amount of eggs eaten were affected by the treatments. Males who consumed eggs had a higher fat percentage than males who did not eat eggs. The result that males with small clutches lost their nests to the crabs supports the idea that eggs are defended only if the benefit from continued care will outweigh the cost and that males therefore are sensitive to the trade-off between present and future reproductive success. Received: 15 May 1997 / Accepted after revision: 15 November 1997     

Sex change limited by paternal care: a test using four Mediterranean labrid fishes,genus Symphodus

Four species of the Mediterrnean wrasse (genus Symphodus) were investigated under natural conditions near Calvi, Corsica, France, to test the idea that extensive male mating-investment limits the extremes of male reproductive success, and thus reduces selection for protogynous sex change. The four species differ in the extent to which males build nests and care for the eggs, and this sort of paternal care can detract from time spent in mating. In S. ocellatus and S. roissali larger males construct an elaborate nest, ventilate the eggs, and engage in territorial defense. The spawning rates for these males are relatively low and variable due to long periods spent in nest construction and egg tending. They also suffer a large amount of interference from smaller males, which may be due to the predictability of nest location. Sex change appears to be absent. S. tinca males construct only a rudimentary nest, do not ventilate the eggs, and experience much less spawning interference. Large males are relatively more successful in mating in this species, and sex change appears to occasionally occur. The large males of S. melanocercus spawn at a much higher rate than small males, due in part to the fact that they do not construct or defend nests and thus are able to spawn on a daily basis. Sex change appears to be common in this species. Thus, the species that shows the greatest sexual difference in changes of expected fertility with size is also the species that shows the strongest expression of sex change. Studies such as this can begin to indicate the actual costs of changing sex.     

Promiscuity: an inbreeding avoidance mechanism in a socially monogamous species?

Summary Paternity likelihood was tested in a population of splendid fairy-wrens Malurus splendens by allozyme electrophoresis. A total of 91 offspring of 24 dams and 37 putative sires were typed at 10 polymorphic loci. All young were compatible with their dams but at least 65% were not fathered by any of the males in their group. A long-term study of this wren population has shown that the males are sedentary, show little evidence of dispersal and help care for the nestlings and fledglings in their group. Had the senior male sired all the offspring in his group, there would have been a high incidence of close inbreeding. The promiscuous mating system demonstrated here would reduce the level of inbreeding in the population but still allow individuals the security of group-living in a stable year-round territory. Offprint requests to: M.G. Brooker     

Egg mimicry and allopaternal care: two mate-attracting tactics by which nesting striped darter (Etheostoma virgatum) males enhance reproductive success

In a variety of fish species with paternal care of offspring, females prefer to spawn in nests that already contain eggs. This female preference has been hypothesized to explain egg thievery in male sticklebacks, allopaternal care of eggs in minnows, and the evolution of egg-mimicking body features in male cichlids and darters. Here we employ microsatellite-based parentage analyses to evaluate the reproductive success of striped darter (Etheostoma virgatum) males that appear to utilize two of these functionally related tactics to entice females to spawn in their nests. In an isolated population (Clear Creek, Ky.), we observed that breeding males develop conspicuous white spots on their pectoral fins. If these spots are egg mimics, as we suspect, then this represents the fourth independent evolutionary origin of egg mimicry documented to date in darters, the first based on pigmentation (as opposed to physical structures), and the first in which the egg mimics vary greatly in number among males. From direct counts of microsatellite genotypes in clutches of embryos, at least 3.8 females contributed to the progeny within a typical nest, and females tended to spawn preferentially with males that were larger and displayed more egg-mimic spots. In another population (Hurricane Creek, Tenn.) without egg mimics, the multi-locus genetic data document that allopaternal care is common, especially among the smallest males who sometimes tend nests containing their own as well as an earlier sire's offspring. Thus, these foster males had adopted egg-containing nests and then successfully spawned with subsequent females. Overall, the genetic data on paternity and maternity, in conjunction with field observations, suggest that egg mimicry and allopaternal care are two mate-attracting reproductive tactics employed by striped darter males to exploit female preferences for spawning in nests with 'eggs'. Electronic Publication     

Intraspecific brood parasitism in the moorhen: parentage and parasite-host relationships determined by DNA fingerprinting

Parasitic female moorhens (Gallinula chloropus) lay from one to six eggs in the nests of conspecific neighbours. DNA fingerprinting was used to show that parasitic eggs could be correctly identified when they appeared in addition to or outside the host’s laying sequence. Moorhen hosts accept all parasitic eggs laid after the 2nd day of their laying period. To understand why moorhen hosts tolerate parasitic eggs, we tested two hypotheses. (1) The quasi-parasitism hypothesis: females lay their eggs in the evening when the host males are normally in attendance at the nest, so host males may allow parasitic females to lay in their nests in exchange for fertilizing their eggs. However, DNA fingerprinting showed that all the parasitic eggs were sired by the parasites’ mates. Parasitic moorhens frequently continue laying a clutch in their own nest, without a break in the laying sequence after a parasitic laying bout. The eggs laid by brood parasites in their own nests were also sired by their own mates. Therefore this hypothesis was rejected. (2) The kin selection hypothesis: if one or both members of the host pair are close relatives of the parasite, the costs of rearing parasitic chicks will be to some degree offset by inclusive fitness benefits. We examined the genetic relationships between parasites and their hosts using DNA fingerprinting and genealogical data. Natal philopatry by both sexes was relatively common in this population, and the probability that a neighbour of either sex was a first-order relative (parent-offspring) was calculated as 0.18. Although first-order relatives were not preferentially chosen as hosts over individuals that were not first-order relatives, even through random host selection there is almost a one-in-five chance that brood parasites in this population are closely related to their hosts. This may facilitate host tolerance of parasitic eggs. Other hypotheses are also discussed. Received: 3 February 1995/Accepted after revision: 27 August 1995     

Egg incubation temperature affects male reproductive success but not display behaviors in lizards

The complex ritualized displays of males in many territorial species suggest that selection has shaped male behaviors in ways that affect fitness. In this study, we evaluated the link between display behavior during male–male interactions and reproductive success in the Australian jacky dragon (Amphibolurus muricatus), a lizard species that uses a complex series of movement patterns for communication. We quantified variation in male display behaviors by using video playback experiments in the laboratory, and subsequently assessed variation in male reproductive success by paternity analyses of offspring. Because the lizards used in this study came from eggs incubated under three thermal environments, we also could evaluate the impact of developmental temperature on adult behavior and reproductive success. Incubation temperature had a strong effect on male reproductive success; males produced under intermediate temperatures sired more offspring than those produced under extreme developmental temperatures. However, incubation temperature did not affect male display behavior, nor was male behavior associated with reproductive success. Our findings do not support the common assumption that display behaviors used during male–male interactions affect reproductive success.