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.     

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.     

The presence of eggs in the nest and female choice in common freshwater gobies (Rhinogobius brunneus)

In many species of fishes with paternal care, females prefer to spawn with males who are already guarding eggs. We studied the effect of egg presence on female mate choice in common freshwater gobies, Rhinogobius brunneus sp. OR. In our tests, females did not prefer males with eggs, suggesting egg presence per se may not act as a cue to attract females. We also examined the effects of brood size on paternal care and offspring survival to look for possible benefits females could obtain when choosing males with eggs. Both fanning by egg-guarding males and egg survival increased with brood size. The presence of neighboring males did have a significantly negative effect on males' parental activity, which subsequently results in a lower level of egg survival than in solitary egg-guarding males. This result provides a partial explanation for the result of eggs not attracting females to mate.     

Filial cannibalism in a nest-guarding fish: females prefer to spawn in nests with few eggs over many

In fish, fecundity correlates with female body size and egg-tending males often eat small broods. Therefore, small females may prefer to spawn in nests that already contain many eggs, to ensure the brood is as large as possible. In contrast, large females may prefer nests with few eggs, if high egg number or density has a negative effect on egg survival, or if there are drawbacks of spawning last in a nest. To test the hypothesis that female body size affects nest (and male mate) choice, using the sand goby (Pomatoschistus minutus), we allowed small and large females to choose between two males that were matched in size — one guarding a small clutch and the other a large clutch, respectively. We recorded where females spawned (measure of female preference), the combined brood size, male courtship, egg care and nest building. We also quantified the effect of brood size and egg density on egg survival in a separate data set. Although the combined broods did not exceed the small brood sizes that are at risk of being eaten, both small and large females preferred to spawn in nests with smaller clutch sizes. This preference could not be explained by more courtship or male parental effort, nor by reduced survival of larger or denser broods. Instead, our result might be explained by females avoiding the danger of cannibalism of young eggs by males or the risk of reduced egg health associated with being near the nest periphery.     

Courtship in fast water currents by a male stream goby ( Rhinogobius brunneus) communicates the parental quality honestly

The stream goby Rhinogobius sp. DA (dark color type) shows exclusive paternal care of the eggs. Males court females in the stream current and previous field observations suggest that females favor males that perform their courtship display in faster water currents, and that such males may have high parental ability because of good physical condition. To validate these observations we examined female choice under controlled laboratory conditions. Mate choice experiments indicated clearly that females preferred males that courted in the faster currents, whereas neither sexually different morphological traits, such as body size, nor the water current alone were important. The experiments with food supply treatments indicated that only males of high physical condition are able to court in the fast currents. Furthermore, males that courted in the fast currents achieved good egg survival, whereas males that were unable to court in the currents did not, due to cannibalism of their egg clutch. Thus, the maximum speed of the water current in which a male courts should be indicative of his quality and of the subsequent survival of eggs under his care. We conclude that Rhinogobius sp. DA females utilize the male courtship display in the water current as an honest indicator of parental quality.Communicated by K. LindströmAn erratum to this article can be found at     

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     

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     

Allopaternal care in the fathead minnow,Pimephales promelas: stepfathers discriminate against their adopted eggs

Summary Some species of fishes with exclusive male parental care exhibit the phenomena of allopaternal care and female preference for males with eggs. In these species, newly reproductive males adopt and care for the eggs of other males, apparently as a part of their mating strategy. Assuming that adoption is adaptive, I would expect males to discriminate between adopted eggs and eggs that they sired themselves. Specifically, I predicted that adopted eggs would receive less care and suffer heavier mortality than sired eggs. I examined the allocation of care and egg survival for adopted and sired eggs in the fathead minnow, Pimephales promelas, and corroborated both predictions.     

Linking male qualities to multiple display traits: an example in a fish with exclusive male care

Recent theoretical models predict that the relative allocation to advertisement and parental care depends on whether paternal care is necessary for offspring survival: In species with exclusive male care, male investment in attraction is expected to reliably indicate paternal care effort and male phenotypic quality. Previous research, yielding contrasting results, has considered how one trait involved in mate attraction interacts with parental care or a specific aspect of male quality. In the blenny Salaria pavo, we perform a comprehensive analysis of the interplay between overall male attractiveness and male quality, the latter in terms of fertility, condition, and parental care. In this fish, males are larger than females, exhibit two sexually dimorphic traits (head crest and anal glands), and solely care for eggs. We generated a male attractiveness index through principal component analyses of morphological traits and quantified parental effort as the total time spent in egg care. In addition, we analyzed the relationships between specific components of attractiveness and male qualities. In agreement with theory predictions, we found that male overall attractiveness is a reliable indicator of fertility, in terms of sperm number, but is unrelated to body condition and parental care effort, with males able to perform high levels of care regardless of their level of advertisement. However, the relative expression of head crest area appears positively related to sperm number but is traded-off with parental care effort. These findings underline the need, in addressing real patterns, to consider interactions between multiple aspects of male display and quality.     

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.     

Factors affecting the allocation of paternal care in waterbugs (Belostoma flumineum Say)

Summary Male giant waterbugs (Belostoma flumineum Say) brood eggs oviposited on their dorsa by conspecific females. Laboratory observations indicate that viable egg pads are occasionally discarded before hatching. Theory predicts that such behavior should occur only if the costs incurred by brooding exceed the benefits of hatching the egg pad. We studied the effects of egg pad size, time invested in brooding, and egg viability upon the continuation of paternal care in the giant waterbug. We found that smaller egg pads are less likely to hatch than larger ones, and males appear to be less likely to discard egg pads as temporal investment increases. However, the inviability of eggs did not appear to affect the probability of an egg pad being discarded. Males of this species appear to have evolved a decision-making process involving the continuation of paternal care. Offprint requests to: K.C. Kruse     

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.     

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     

Local mate competition and precise sex ratios in Telenomus fariai (Hymenoptera: Scelionidae), a parasitoid of triatomine eggs

Telenomus fariai is a gregarious endoparasitoid of the eggs of several species of Triatominae (Hemiptera) with a high degree of sibmating: males fertilize their sisters inside the host egg before emergence or emerge first and copulate with their sisters as these emerge. Our results show that, when laying alone, T. fariai behaves adaptively, minimizing offspring mortality and conforming to the prediction of local mate competition (LMC) theory by laying a single male, which is sufficient to fertilize all the sisters. When more than one wasp was placed with one host, sex ratios still conformed to LMC predictions but, despite the decreasing number of eggs laid per wasp, clutch size could not be completely adjusted to avoid mortality. This is not surprising, as superparasitism is rare in the field. Offspring production was independent of the contacts between conspecifics but was affected by the number of mothers laying on a single host egg. The sex of the progeny was precisely determined: a female produced one male per clutch when laying on both unparasitized or previously parasitized hosts. On the other hand, a mother produced less daughters when superparasitizing. Under crowded conditions, the number of eggs laid per female wasp and per host decreased as the number of mothers increased. Developmental mortality also increased with the number of T. fariai eggs per host, determining a maximum of approximately 14 emerged adults. Host resources per individual affected male and female adult size with similar intensity, and male adult mortality was slightly higher than that for females. These results, and previous findings, suggest that T. fariai attains Hamiltonian sex ratios by laying one male and a variable number of females, and that the detection of chemical marks left by conspecifics provides information on the number of foundresses sharing a patch. Received: 4 February 2000 / Received in revised form: 19 April 2000 / Accepted: 20 May 2000     

Within-clutch egg size asymmetry covaries with embryo sex in the yellow-legged gull Larus michahellis

Non-random sex allocation may occur whenever the expected reproductive value of sons and daughters differs, as is the case when the sexes differ in susceptibility to environmental conditions or maternal effects (e.g. egg size and hatch order). Under such circumstances, covariation between egg and clutch characteristics and egg sex may be expected, and this covariation should vary with maternal state or ecological conditions. In this 2-year study (2007–2008), we examined sex allocation in relation to egg and clutch traits in the yellow-legged gull Larus michahellis, a species where male chicks are larger and more susceptible to harsh rearing conditions than female ones. In 2008, eggs were more likely male early in the season in two- but not three-egg clutches, and large eggs were more likely males late in the season. No egg/clutch traits predicted egg sex in 2007. Within-clutch egg mass asymmetry (the difference in egg mass between the first- and last-laid eggs) predicted sex in both years. In 2007, clutches with smaller egg mass variation were more likely to contain males, while in 2008 this relationship held for the last-laid egg and was reversed for the preceding egg(s). Laying order and sex of the previous egg did not predict egg sex, providing no evidence of sex-specific oocyte clustering. Thus, the relationships between egg sex and egg/clutch traits differed among years, suggesting a phenotypically plastic response of females to extrinsic conditions, and involved within-clutch egg mass asymmetry, a trait likely reflecting variation in maternal quality and/or reproductive tactics, which has been largely neglected in previous studies of sex allocation.     

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     

Yolk hormones and sexual conflict over parental investment in the pied flycatcher

Female birds might be able to manipulate the parental effort of their male partner through elevated transfer of hormones to the eggs, since these hormones affect many chick traits that males might use as cues for adjusting the level of their investment. We experimentally studied whether female pied flycatchers Ficedula hypoleuca could manipulate male investment via yolk androgens. There is much more variation in yolk androgen levels between females than within clutches, and in order to change the androgen levels of the eggs, we swapped whole clutches between nests. To estimate the androgen levels of the clutch, we measured the androgen content of a single egg per clutch. Females did not succeed in manipulating male effort using yolk androgens, since there was no relationship between the division of parental care within a pair and either original or foster egg androgen levels. One of these relationships should have occurred if females were manipulating males. The proportion of feeding visits by the male was higher when the male was old (55%) than when he was young (45%) and females laid eggs with higher androgen levels when mated with a young male. Young males did not exhibit any responses to yolk androgen levels either, which indicates that females cannot exploit their effort more than that of old males. We suggest that females may allocate yolk androgens to adjust the growth trajectories of the chicks to poor growing conditions when mated with young males that are poor providers or occupying a poor territory.     

Male reproductive success in two midwife toads,Alytes obstetricans and A. cisternasii

Summary One population of the midwife toad species Alytes obstetricans and one of A. cisternasii were studied in Spain for two consecutive reproductive seasons. Males that were most successful at hatching a high proportion of their clutch did not obtain more matings. On the other hand, in both species larger body size conferred a significant reproductive advantage on males. These results are explained mainly by the increased number of mates obtained by larger males, probably as a result of female choice. The selection gradients for body size in males (regressions of reproductive success on body size) were not significantly different within species between years nor between species within the same period of time. Hatching success (proportion of the eggs hatched) was not correlated with male body size in A. obstetricans. Hatching success in A. cisternasii was weakly negatively correlated with male body size in 1988.     

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.     

Reproductive biology of deep-water calanoid copepods from the Arctic Ocean

Reproductive modes and egg production were studied in 15 species of meso- and bathypelagic copepods from nine Calanoida families in the Arctic Ocean. During shipboard incubation, females of seven species released eggs freely into the water and females of three species produced membrane-bound egg sacs. One species, Aetideopsis rostrata, produced a mass of eggs looking like an egg sac, but the “sac” lacked a membrane and disintegrated within 2 h. Females of four additional species were encountered with membrane-bound egg sacs in the preserved samples. In most families, only one reproductive mode, either egg-carrying (the Euchaetidae, Augaptilidae), or broadcast spawning (the Heterorhabdidae, Spinocalanidae, Scolecitrichidae, Tharybidae, Bathypontiidae) was observed. In contrast, different genera of the Aetideidae family demonstrated different reproductive modes, with broadcast spawning predominant in the benthopelagic species, and both broadcast spawning and egg-brooding in the planktonic species. Clutch size and egg diameter varied widely between species in both broadcast spawners and egg-brooders. In broadcast spawners, the clutch size varied from 1 to 95 eggs female⁻¹, while the average egg diameter ranged from 152 to 440 μm. The clutch size for egg brooders varied between 3 and 82, while average egg diameter varied from 258 to 732 μm. Deep-water broadcast spawners produced much larger eggs compared to surface-dwelling broadcast spawning species. This larger egg size may result in a reduction, or elimination, of feeding during naupliar stages, thereby improving the survival potential of deep-water species.