Alloparental care in the sea: Brood parasitism and adoption within and between two species of coral reef Altrichthys damselfish?

The evolution of parental care opens the door for the evolution of brood parasitic strategies that allow individuals to gain the benefits of parental care without paying the costs. Here we provide the first documentation for alloparental care in coral reef fish and we discuss why these patterns may reflect conspecific and interspecific brood parasitism. Species‐specific barcodes revealed the existence of low levels (3.5% of all offspring) of mixed interspecific broods, mostly juvenile Amblyglyphidodon batunai and Pomacentrus smithi damselfish in Altrichthys broods. A separate analysis of conspecific parentage based on microsatellite markers revealed that mixed parentage broods are common in both species, and the genetic patterns are consistent with two different modes of conspecific brood parasitism, although further studies are required to determine the specific mechanisms responsible for these mixed parentage broods. While many broods had offspring from multiple parasites, in many cases a given brood contained only a single foreign offspring, perhaps a consequence of the movement of lone juveniles between nests. In other cases, broods contained large numbers of putative parasitic offspring from the same parents and we propose that these are more likely to be cases where parasitic adults laid a large number of eggs in the host nest than the result of movements of large numbers of offspring from a single brood after hatching. The evidence that these genetic patterns reflect adaptive brood parasitism, as well as possible costs and benefits of parasitism to hosts and parasites, are discussed.     

Fine-tuned modulation of competitive behaviour according to kinship in barn swallow nestlings

Kin selection theory predicts that, in species where progeny members compete for limiting parental care, individual offspring should be more prone to monopolize parental resources as their genetic relatedness to brood competitors decreases. Mixed parentage among broodmates may arise as a consequence, for example, of extra-pair fertilization or brood parasitism events. In this experimental study of barn swallows (Hirundo rustica), we reciprocally partially cross-fostered hatchlings between broods and compared the behaviour of pairs of related and unrelated broodmates in a competitive context, both under normal food provisioning regime and after mild food deprivation. We found that scramble competition for food mediated by visual and vocal solicitation displays (begging) is inversely related to relatedness among competitors, independent of their level of satiation. Nestlings may modulate their competitive behaviour according to vocal cues that vary with their origin and allow kin recognition. We also uncover direct fitness costs to both parents and offspring arising from mixed parentage in a brood, in terms of increased parental workload and reduced survival of the nestlings. Such previously neglected costs may select for reduced frequency of extra-pair fertilizations and brood parasitism in species with extensive parental care.     

Diverse parentage relationships in paternal mouthbrooding fishes

While mouthbrooding is not an uncommon parental care strategy in fishes, paternal mouthbrooding only occurs in eight fish families and is little studied. The high cost of paternal mouthbrooding to the male implies a low risk of investment in another male''s offspring but genetic parentage patterns are poorly known for paternal mouthbrooders. Here, we used single-nucleotide polymorphism genetic data to investigate parentage relationships of broods of two mouthbrooders of northern Australian rivers, mouth almighty Glossamia aprion and blue catfish Neoarius graeffei. For N. graeffei, we found that the parentage pattern was largely monogamous with the brooder male as the sire. For G. aprion, the parentage pattern was more heterogeneous including observations of monogamous broods with the brooder male as the sire (73%), polygyny (13%), cuckoldry (6%) and a brood genetically unrelated to the brooder male (6%). Findings demonstrate the potential for complex interrelationships of male care, paternity confidence and mating behaviour in mouthbrooding fishes.     

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

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

Male "mixed" reproductive strategies in biparental species: Trivers was probably right, but why?

Trivers proposed that, if parental care by both sexes is advantageous, males should practice a "mixed" strategy of seeking extrapair copulations, while restricting their parental investment to offspring of social mates. We explore circumstances under which males should limit their parental care in the predicted manner. We find that Trivers's "mixed" strategy will generally be evolutionarily stable so long as either socially monogamous or polygynous males usually sire more offspring per brood from a social mate than they typically sire in broods of extrapair mates. Polygynous males should spread investment across their home nests unless the expected number of chicks sired in them differs widely. Whether polygynous males should restrict paternal care to social mates' offspring hinges additionally on resident male investment in broods containing extrapair young: if resident males contribute minimally, some investment by a polygynous extrapair male becomes more advantageous. Recently reviewed data on extrapair fertilization distributions within monogamous and polygynous passerines suggest that extrapair offspring often predominate numerically within their broods, consistent with sperm expenditure theory. Nevertheless, most species conform to the model's criterion regarding relative parentage levels in broods of social versus extrapair mates. Patterns of extrapair parentage thus appear sufficient to stabilize biparental care systems.     

Serial monogamy in the European long-snouted seahorse Hippocampus guttulatus

Seahorses (Hippocampus spp.) are non-sex-role-reversed members of the Syngnathidae family that provide extensive brood care. Previous studies of seahorses have revealed monogamy within a single brood, but their longer term mating system had not been comprehensively evaluated. The parental contribution to 29 wild-born broods of Hippocampus guttulatus, sampled from six Portuguese populations with differing seahorse densities and sex ratios, was assessed using microsatellite DNA markers. To assess the longer term genetic mating system of this species parentage was determined in eleven broods sampled from a captive population over two breeding seasons. Genetic data suggest that this socially polygamous seahorse is serially monogamous across breeding seasons, i.e. monogamous within a season but may switch mates between seasons, and that differing population densities and sex ratios do not affect the mating system.     

The importance of genetic evidence for identifying intra-specific brood parasitism

Intra-specific brood parasitism is widespread among birds. When genetic evidence is not available, criteria like super-normal clutch size, high within-clutch variance in egg morphology, and shorter than normal laying intervals have been used to identify parasitized broods. Here we report genetically determined parentage of a clutch of super-normal size in a species with fixed clutch size, the northern lapwing Vanellus vanellus . Results from multi-locus DNA fingerprinting revealed no loss of parentage in this brood. Furthermore, no loss of parentage was found in another clutch with a high variance in egg size and colouration. These findings add to previous evidence that reliable classification of brood parasitism requires molecular analysis.     

Genetic evidence for prevalence of alloparental care in a socially monogamous biparental cichlid fish,Perissodus microlepis,from Lake Tanganyika supports the “selfish shepherd effect” hypothesis

Alloparental care – care for unrelated young – is rare in animals, and its ecological or evolutionary advantages or, alternative maladaptive nature, remain unclear. We investigate alloparental care in the socially monogamous cichlid fish Perissodus microlepis from Lake Tanganyika that exhibits bi‐parental care. In a genetic parentage analysis, we discovered a surprisingly high percentage of alloparental care represented by brood mixing, extra‐pair paternity and extra‐pair maternity in all broods that we investigated. The percentage of nondescendant juveniles of other parents, i.e., brood mixing, ranged from 5% to 57% (mean = 28%). The distribution of genetic parentage also suggests that this socially monogamous species has, in fact, polygamous mating system. The prevalence of genetically mixed broods can be best explained by two, not mutually exclusive hypotheses on farming‐out and fostering behaviors. In the majority of broods, the sizes of the parents’ own (descendant) offspring were significantly larger than those of the adopted (nondescendant) juveniles, supporting the ‘selfish shepherd effect’ hypothesis, i.e., that foster parents preferentially accept unrelated “smaller or not larger” young since this would tend to lower the predation risks for their own larger offspring. There was also a tendency for larger parents particularly mothers, more so than smaller parents, to care predominantly for their own offspring. Larger parents might be better at defending against cuckoldry and having foreign young dumped into their broods through farming‐out behavior. This result might argue for maladaptive effects of allopatric care for the foster parents that only larger and possibly more experienced pairs can guard against. It needs to be determined why, apparently, the ability to recognize one's own young has not evolved in this species.     

High frequency of multiple paternity in broods of a socially monogamous cichlid fish with biparental nest defence

In several animal taxa, genetic analyses have demonstrated that social monogamy and biparental brood care do not preclude polygamous reproduction. Few studies have been conducted in fish, but in fish species without alternative reproductive phenotypes, social monogamy was largely congruent with genetic parentage. In contrast to these findings, we report an exceptionally high level of multiple paternity in a socially monogamous cichlid fish with biparental nest defence ( Variabilichromis moorii ), inferred from microsatellite and mitochondrial data of 10 broods. Whereas all offspring in a nest shared a common mother, each brood was sired by 2 to > 10 males. None of the inferred sires was assigned a large proportion of the brood. Paternity was estimated as the minimum number of sires required to explain multilocus offspring genotypes, and as the maximum-likelihood number of sires given population allele frequencies. Analysis of simulated brood genotypes suggested that, although these two methods tend to under- and overestimate, respectively, the true number of sires, primary sires with many offspring in a brood would have been detected. Hence, the genetic data indicate that the nest tending males suffer substantial cuckoldry and provide alloparental care for a large number of unrelated fry. We have no data on the social status of the cuckolding males, but due to synchronous spawning of pairs and commitment to brood care of paired males, it is possible that most of the parasitic spawners are solitary males.     

Brood size and the economy of brood defence: examining Lack's hypothesis in a biparental cichlid fish

Synopsis We tested the explanatory value of two hypotheses reviewed by Lack (1954) in the maintenance of brood size in free-ranging convict cichlidsCichlasoma nigrofasciatum: (1) physiological constraints on egg production, and (2) behavioural constraints imposed by brood defence. Number of free-swimming young in 13 experimental (E) broods was augmented to the upper limit of the size distribution of natural broods (150 young); 18 control (C) broods were handled in the same way but brood size was not changed (mean ± SE = 69.5 ± 11.0). E and C brood sizes were measured at 5 day intervals. At day 20 (just before independence from parental care), 50.3 ± 9.4 (n = 9) young remained in E broods and 30.8 ± 7.8 (n = 8) young remained in C broods (p> 0.05). Offspring number did not differ significantly (p> 0.05) between C and E broods after day 10. Mean growth rate of offspring was significantly lower in E broods than in C broods, perhaps in response to increased density of young in the former. Both the convergence of offspring number in E and C broods and suppression of growth in E broods support a behavioural constraint; that during the first 10 days in which the young are free swimming, two parents are unable to defend large broods as successfully as small broods. A trade-off exists in parental investment between current and future reproduction. Extra-parental investment in current reproduction (eggs) does not result in an increased number of young at independence, therefore a behavioural constraint during brood defence should stabilize the evolution of clutch size.     

The effect of brood size and age on partial filial cannibalism in the scissortail sergeant

Within the size range found in the field for the scissortail sergeant Abudefduf sexfasciatus , there was no correlation between the number of cannibalized eggs and total brood size. Very small broods were fully cannibalized. In a manipulation experiment, males were provided with broods of one of three standardized sizes: at the two extremes and in the middle of the range of naturally occurring broods. Brood size had no effect on partial filial cannibalism, but parental effort increased with increasing brood size. Field correlates and the manipulation experiment showed that the cost of cannibalism in terms of current reproductive success decreased significantly with increasing brood size. Contrary to expectations, there was no relationship between male size and the incidence of cannibalism. No preference for younger eggs was found either from field correlates or from a manipulative experiment in which males were provided with an equal number of young and old eggs at the beginning of the parental phase.     

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

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

Brood size modifications affect plumage bacterial assemblages of European starlings

During reproduction, birds face trade-offs between time and energy devoted to parental effort and traits associated with self-maintenance. We manipulated brood sizes to investigate the effects of such trade-offs on feather bacterial densities and the structure of bacterial assemblages on feathers in adult European starlings, Sturnus vulgaris, and in vitro feather degradation. As predicted by a trade-off between parental effort and self-maintenance, we found that birds with enlarged broods had more free-living bacteria on their feathers than birds with reduced broods. Furthermore, we found a significant interaction between brood manipulation and original brood size on free-living bacterial densities suggesting that the trade-off is mediated by the adults' initial reproductive investment. In contrast, brood size manipulations had no significant effect on densities of attached bacteria. Using ribosomal intergenic spacer analysis (RISA), we demonstrated that brood manipulations significantly modified the structure (band pattern) of feather-degrading bacterial assemblages, but had no significant effect on their richness (number of bands) or the in vitro feather degradation. In vitro feather degradation varied in relation to the premanipulation brood size and positively with the richness of the feather degrading bacterial community. Besides brood manipulation effect, we found that ecological factors and individual traits, such as the age, the nest location or the capture date, shaped bacterial assemblages and feather degradation capacities.     

Patterns of multiple paternity and maternity in fishes

The characterization of patterns of multiple mating is a major facet of molecular ecology and is paramount to understanding the evolution of behaviours associated with parental care and mate choice. Over the last 15 years, fishes have been particularly well studied with respect to multiple maternity and paternity thanks to the widespread application of microsatellite markers. The present review focusses on the impressive literature on genetic parentage in fishes. In studies of natural populations, we find that multiple paternity is extremely common across fish species, whereas rates of multiple maternity are much more variable. In species with nest defence, for example, rates of multiple maternity are strongly bimodal, and the occurrence of multiple dams per brood is either rare or the rule. The sex of the care‐giving parent is correlated with the rate of multiple parentage: when males provide uniparental care, rates of multiple paternity are low compared to rates of multiple maternity; when females provide parental care, either alone or assisted by males, rates of multiple paternity are highly variable, whereas rates of multiple maternity are quite low. These patterns may reflect conflicts between the reproductive interests of males and females. We also find that fishes in which females brood the offspring internally display much higher rates of multiple paternity compared to mammals or birds, whereas reptiles are intermediate. Male‐nesting fish species, however, show rates of multiple paternity more similar to those found in other vertebrates. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 735–760.     

Cooperation, conflict, and crèching behavior in goldeneye ducks

Crèching behavior, or brood amalgamation, results in offspring being reared by adults other than their genetic parents. Although a variety of hypotheses have been proposed to explain this behavior, most assume either that brood amalgamation is accidental (i.e., nonselected) or that adoption of young is selected for because of social benefits to the young and/or adopting parents. We propose, instead, that brood amalgamation is a function of two separate processes: brood desertion and brood adoption. To examine brood desertion, we develop a graphic model to predict when parents should abandon their young and we test this model experimentally for the Barrow's goldeneye (Bucephala islandica). As predicted, females deserted their offspring when the size of the brood was experimentally reduced. Brood adoption occurred when deserted ducklings joined other broods. However, the success of ducklings in doing so was strongly dependent on the availability of potential host broods and on the age of the recipient broods. Foreign ducklings were readily accepted into young broods (<10 d old) but invariably were rejected from old broods. We could detect no benefits or costs of brood adoption to the host females, contrary to the expectations of a social benefit hypothesis. Our experiments indicate that Crèching behavior is driven by selection on adults to abandon their brood when the benefits of continued investment are outweighed by the reduction in future reproduction and selection on deserted ducklings to join other broods to obtain parental care. Rather than a form of cooperative brood care, Crèching in goldeneyes is perhaps best considered as a form of reproductive parasitism, entailing parent-offspring conflict over brood desertion and intergenerational conflict over adoption of abandoned young.     

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

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

Variation in multiple paternity in natural populations of a free-spawning marine invertebrate

For free-spawning marine invertebrates, fertilization processes control the genetic diversity of offspring. Each egg can potentially be fertilized by a sperm from a different male, and hence genetic diversity within a brood varies with levels of multiple paternity. Yet, few studies have characterized the frequency of multiple paternity in natural spawns. We analysed patterns of multiple paternity in two populations of the colonial ascidian Botryllus schlosseri using microsatellites. Because previous studies have shown that at moderate to high population densities, competition among male-phase B. schlosseri colonies results in the nearest male dominating the paternity of a brood, we specifically tested the effect of population density on patterns of paternity. Paternity was estimated using three multilocus indices: minimum number of fathers, counts of sperm haplotypes, and effective paternity (K(E)). Multiple paternity was evident in more than 92% of the broods analysed, but highly variable, with a few broods displaying unequal contributions of different males. We found no effect of population density on multiple paternity, suggesting that other factors may control paternity levels. Indirect benefits from increasing the genetic diversity of broods are a possible explanation for the high level of multiple paternity in this species.     

Extrapair paternity in a flock-living passerine, the vinous-throated parrotbill Paradoxornis webbianus

Understanding the factors that affect the occurrence of extrapair paternity (EPP) is one of the central issues in sexual selection. We investigated genetic parentage and the ecological factors affecting patterns of EPP in the vinous-throated parrotbill, Paradoxornis webbianus , a flock-living species with double broods. Using microsatellite DNA fingerprinting, we determined parentage of 246 offspring in 50 broods over two years (2005 and 2006). Nineteen offspring (8%) from 13 broods (26%) were sired by extrapair males and one offspring (0.4%) was probably the result of intraspecific brood parasitism. The prevalence of EPP varied significantly through the breeding season: 95% of broods with EPP (12/13) occurred in the first of two laying peaks. Parentage assignment revealed that half of extrapair males (6/12) were adjacent neighbours. The distribution of EPP was not significantly related to the ecological factors including breeding density and breeding synchrony. Instead, we suggest that social characteristics such as flocking and weak territoriality may determine the observed pattern of EPP in this study.     

Parentage and the evolution of parental behavior

Parentage is the proportion of juveniles in a brood that areoffspring of potential care givers. We analyzed how reductionsin parentage affect the evolution of parental behavior usinga static optimization model. The main benefit of parental effortwas an increase in the survival of offspring, and the main costswere reduced opportunities to seek additional matings or toparasitize neighbors and or reduced survival. Both the costsand benefits included terms for relatedness to young. The effectof parentage depended on (1) whether parents responded in ecologicaltime (facultative response) or in evolutionary time (nonfacultativeresponse), (2) whether the cues enabling assessment of parentagepermitted discrimination among offspring, and (3) whether parentagewas the same among different groups of juveniles (unrestricted)or varied between them (restricted). When parents did not knowtheir own parentage and mean parentage was the same for allmatings, reduced parentage affected the costs and benefits equally,so, as in several previous models, there was no effect on theoptimal level of parental effort. Parentage did affect optimalparental effort when mean parentage to the present brood differedfrom that to young from alternative or future matings. Loweredparentage reduced optimal parental effort when the cost of parentingwas missed opportunities for extrapair copulations or broodparasitism or when parentage was consistently higher in alternativeor future matings. Nonlinear changes in parentage with age gavecomplex trajectories of parental care, with individuals of differentages having similar parentage but exhibiting different levelsof parental effort. Correlations between parentage and othervariables in the model (such as opportunities for additionalmatings) sometimes masked, but never eliminated, the effectsof parentage. When parents could discriminate their own youngin a brood, overall parental effort was reduced, but nepotismwas increased. When parents could not discriminate their ownoffspring but had general cues about average parentage to thebrood, effects varied depending on the costs and benefits ofparental behavior. When parental behavior was costly to caregivers, parentage had more effect than when parenting was notcostly. Likewise, parentage had less effect when care greatlyincreased offspring survival than when care was less necessary.Our analyses reconcile conflicting results from previous modelsand suggest a general framework for analyzing parental behaviorwithin populations and among higher taxonomic groups.     

Extra-pair paternity does not result in differential sexual selection in the mutually ornamented black swan (Cygnus atratus)

We studied patterns of parentage in 85 broods (332 cygnets) of black swans during three breeding seasons, using a set of eight polymorphic microsatellite markers. We detected both intraspecific brood parasitism (IBP; < 5% of cygnets per year) and extra-pair paternity (EPP). In these years, 10-17% (mean = 15.1%) of cygnets resulted from EPP, and 27-40% (mean 37.6%) of broods contained at least one extra-pair cygnet. Compared with levels of EPP in closely related species with similar life histories, these values are unexpectedly high. EPP in black swans appears unrelated to ecological factors (breeding density and synchrony) or genetic factors (genetic similarity between pair members or genetic quality of the offspring). We found no evidence that a mutual sexual feather ornament known to play a role in social mate choice in black swans (curled wing feathers) is involved in extra-pair mate choice. EPP does not lead to greater variance in reproductive success in males, relative to females in this species. We therefore suggest that EPP does not result in differential sexual selection on males and females, explaining why they are ornamented to the same degree.