Parental investment with a superior alien in the brood

When a parent's parentage differs across breeding attempts, established theory predicts that the parent should invest more in a brood when perceived parentage is high. We present a model of parental investment in which offspring unrelated to the parent have a competitive advantage over the parent's own offspring and take a larger share of investment. We show that this can weaken or, if the competitive advantage is great, reverse the predicted relationship between perceived parentage and parental investment. A moderate competitive advantage of extra-pair young over within-pair young could partly explain the lack of any clear relationship between paternal care and paternity in many studies, and could easily arise if females choose extra-pair partners for good genes. Our results are also relevant to interspecific avian brood parasitism. As parasites reared together with host offspring are often superior competitors, their hosts could benefit from increasing investment in response to suspected parasitism.     

Barn swallow chicks beg more loudly when broodmates are unrelated

Parents of a variety of animal species distribute critical resources among their offspring according to the intensity of begging displays. Kin selection theory predicts that offspring behave more selfishly in monopolizing parental care as relatedness with competitors declines. We cross-fostered two eggs between barn swallow (Hirundo rustica) clutches and compared the loudness of begging between mixed and control broods under normal feeding conditions and after a period of food deprivation. Begging loudness was higher in mixed broods under normal but not poor feeding conditions. Survival was reduced in mixed than control broods. Call features varied according to parentage, possibly serving as a cue for self-referent phenotype matching in mixed broods. This is the first evidence within a vertebrate species that competitive behaviour among broodmates depends on their relatedness. Thus, kin recognition and relatedness may be important determinants of communication among family members, care allocation and offspring viability in barn swallows.     

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.     

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.     

Strict monogamy in a semi-colonial passerine: the Jackdaw Corvus monedula

In this study we used DNA fingerprinting to provide an accurate measure of paternity in a nest-box colony of Jackdaws. The species is a semi-colonial, socially monogamous passerine which establishes long-term pair bonds. Parents raise a single annual brood in which 50% brood reduction is commonplace. However, nest sites are a limited resource, non-breeding adults are also common around colonies and males are frequently separated from their incubating females during the fertile egg-laying period so that opportunities arise for extra-pair copulation. The parentage analysis, however, revealed no cases of extra-pair fertilisation (EPF) or intra-specific brood parasitism. Therefore fledgling output or survival is likely to be a good measure of individual reproductive success in this species. The lack of EPFs is not explained by nesting synchrony and we discuss the relative costs and benefits to females of seeking EPFs; the likelihood that paternal care and a life-history strategy similar to many long-lived non-passerines may also constrain the species to monogamy.     

Begging and cowbirds: brood parasites make hosts scream louder

Avian brood parasites have evolved striking begging abilitythat often allows them to prevail over the host progeny in competitionfor parental resources. Host young are therefore selected bybrood parasites to evolve behavioral strategies that reducethe cost of parasitism. We tested the prediction that the intensityof nestling begging displays functioning to attract parentalcare increases across species with the frequency of parasitismby the brown-headed cowbird (Molothrus ater). This was expectedbecause host young should try to prevail over highly competitiveparasitic broodmates in scramble interactions, act more selfishlywhen frequency of parasitism is high because brood parasitesoften affect more severely host condition than conspecific broodmates,and discount the kin selection costs of subtracting resourcesto unrelated parasites. Across 31 North American host species,begging loudness positively covaried with parasitism rate inPasserines, and such effect was stronger in species with smallcompared with large clutches. Begging loudness increased withbrood parasitism and nest predation among the most suitablehost species. These results held after controlling for concomitantecological factors and for common ancestry effects. Our resultssupport the hypothesis that avian brood parasitism has playeda role in the evolution of begging behavior of host young.     

Pedigree simulations reveal that maternity assignment is reliable in populations with conspecific brood parasitism,incomplete parental sampling and kin structure

Modern genetic parentage methods reveal that alternative reproductive strategies are common in both males and females. Under ideal conditions, genetic methods accurately connect the parents to offspring produced by extra-pair matings or conspecific brood parasitism. However, some breeding systems and sampling scenarios present significant complications for accurate parentage assignment. We used simulated genetic pedigrees to assess the reliability of parentage assignment for a series of challenging sampling regimes that reflect realistic conditions for many brood-parasitic birds: absence of genetic samples from sires, absence of samples from brood parasites and female kin-structured populations. Using 18 microsatellite markers and empirical allele frequencies from two populations of a conspecific brood parasite, the wood duck (Aix sponsa), we simulated brood parasitism and determined maternity using two widely used programs, cervus and colony . Errors in assignment were generally modest for most sampling scenarios but differed by program: cervus suffered from false assignment of parasitic offspring, whereas colony sometimes failed to assign offspring to their known mothers. Notably, colony was able to accurately infer unsampled parents. Reducing the number of markers (nine loci rather than 18) caused the assignment error to slightly worsen with colony but balloon with cervus . One potential error with important biological implications was rare in all cases—few nesting females were incorrectly excluded as the mother of their own offspring, an error that could falsely indicate brood parasitism. We consider the implications of our findings for both a retrospective assessment of previous studies and suggestions for best practices for future studies.     

Mother guarding: how offspring may influence the extra-pair behaviour of their parents

In this paper we propose a novel form of social control of mate choice. Through mother guarding, offspring can help in protecting the paternity of their father by preventing their mother from engaging in extra-pair matings. We present a model that predicts the circumstances under which mothers should be selected to seek or avoid extra-pair matings, and existing offspring should be selected to prevent or promote such matings. In its simplest form, our model shows that offspring are selected to mother guard as long as the viability of extra-pair young is less than twice that of within-pair young; when the relative viability is greater, offspring are selected to promote extra-pair mating by their mother. If the existing offspring are not necessarily sired by their mother's social mate, then the potential for conflict is further reduced. We also consider whether offspring have an interest in the extra-pair reproduction of their fathers. We show that when the costs of the father's infidelity to the mother's brood are high, existing offspring are selected to prevent extra-pair mating by their father; when such costs are low, offspring are selected to promote extra-pair mating by their father. In principle, our model applies to all species where offspring show delayed dispersal and where breeding pairs raise multiple broods or litters. This situation exists in, but is not limited to, the majority of cooperatively breeding species. The significance of this model with regard to our current understanding of the evolution of extra-pair behaviour in such species is discussed.     

Relatedness and the evolution of conspecific brood parasitism

In conspecific brood parasitism (CBP), a parasitic female takes advantage of the parental care performed by a host female by laying eggs in the nest of the host. The host female raises the offspring of the parasitic female as well as her own. In species where local females are related, direct costs for the host might be more than compensated for by gains in inclusive fitness through increased reproduction of a related parasite, but the role of relatedness in CBP is debated. This inclusive-fitness model of parasitism, structured as a game between host and parasite, suggests that both females can gain inclusive fitness and that host-parasite relatedness can therefore facilitate the evolution of CBP. Crucial assumptions are that there is kin discrimination and a potential for host resistance to parasitism by unrelated females but close relatives are accepted. The cost of parasitism in terms of reduced clutch size or offspring survival for the host must not be large; otherwise, parasitism will reduce her inclusive fitness. Therefore, if these costs are high, it does not benefit a host to accept a parasite, even if the parasite is closely related. The secondary female may still have higher fitness from parasitism, but if the costs are high, she should parasitize an unrelated host, not a relative. This requires that the reduction in parasite success that a host can cause by resistance is not too large; otherwise, it will be better for the secondary female to parasitize an accepting related host or to nest solitarily. For these reasons, host-parasite relatedness is most likely to occur in animals where costs of being parasitized are low and host resistance can markedly reduce the success of an unrelated parasite. When costs are higher, parasitism of unrelated hosts may be better, and if host resistance strongly reduces parasite success, solitary breeding is preferable. In some cases, CBP is directly advantageous for the host, and it may sometimes evolve in close connection with cooperative breeding, which is also considered in the model. Some but not all empirical results support these ideas, and more detailed studies of behavior, relatedness, and reproduction of host and parasite are needed for critical tests.     

When should cuckolded males care for extra-pair offspring?

In socially monogamous species with bi-parental care, males suffer reduced reproductive success if their mate engages in extra-pair copulations (EPCs). One might therefore expect that males should refuse to care for a brood if they can detect that an EPC has occurred. Here, we use a game-theory model to study male brood care in the face of EPCs in a cooperatively breeding species in which offspring help to raise their (half-) siblings in their parents' next breeding attempt. We show that under certain conditions males are selected to care even for broods completely unrelated to themselves. This counterintuitive result arises through a form of pseudo-reciprocity, whereby surviving extra-pair offspring, when helping to rear their younger half-siblings, can more than compensate for the cost incurred by the male that raised them. We argue that similar effects may not be limited to cooperative breeders, but may arise in various contexts in which cooperation between (half-) siblings occurs.     

Within-brood competition and the optimal partitioning of parental investment

In this article, we introduce a simple within-brood competitive growth model that maximizes parental fitness in unpredictable food conditions in species that exhibit parental care, progressive provisioning, and an initial brood overproduction. We argue that competition between siblings may provide a proximate mechanism for parents to adjust the number of surviving offspring or the social organization of the group in social species to food conditions.     

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

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

Coevolution of female fidelity and male help in populations with alternative reproductive tactics

In socially monogamous species, pair-bonded males often continue to provide care to all offspring in their nests despite some degree of paternity loss due to female extra-pair copulation. Previous theoretical models suggested that females can use their within-pair offspring as ‘hostages'' to blackmail their social mates, so that they continue to provide care to the brood at low levels of cuckoldry. These models, however, rely on the assumption of sufficiently accurate male detection of cuckoldry and the reduction of parental effort in case of suspicion. Therefore, they cannot explain the abundant cases where cuckolded males continue to provide extensive care to the brood. Here we use an analytical population genetics model and an individual-based simulation model to explore the coevolution of female fidelity and male help in populations with two genetically determined alternative reproductive tactics (ARTs): sneakers that achieve paternity solely via extra-pair copulations and bourgeois that form a mating pair and spend some efforts in brood care. We show that when the efficiency of mate guarding is intermediate, the bourgeois males can evolve to ‘specialize'' in providing care by spending more than 90% of time in helping their females while guarding them as much as possible, despite frequent cuckoldry by the sneakers. We also show that when sneakers have tactic-specific adaptations and thus are more competitive than the bourgeois in gaining extra-pair fertilizations, the frequency of sneakers and the degrees of female fidelity and male help can fluctuate in evolutionary cycles. Our theoretical predictions highlight the need for further empirical tests in species with ARTs.     

Genetic perspectives on the natural history of fish mating systems

Molecular analyses of bird and mammal populations have shown that social mating systems must be distinguished from genetic mating systems. This distinction is important in fishes also, where the potential for extrapair spawning and intraspecific brood parasitism is especially great. We review studies on fishes that have used molecular markers to document biological parentage and genetic mating systems in nature, particularly in species with extended parental care of offspring. On average, nest-guarding adults parented about 70-95% of their custodial offspring, and approximately one-third of the nests were cuckolded to some extent. Furthermore, nearly 10% of the assayed nests contained offspring tended by foster fathers either because of nest takeovers or egg thievery. On average, fish that provide parental care on nests spawned with more mates than did fish with internal fertilization and pregnancy. Overall, genetic markers have both confirmed and quantified the incidence of several reproductive and other social behaviors of fishes, and have thereby enhanced our knowledge of piscine natural history.     

With a little help from my kin: barn swallow nestlings modulate solicitation of parental care according to nestmates' need

In altricial species, offspring competing for access to limiting parental resources (e.g. food) are selected to achieve an optimal balance between the costs of scrambling for food, the benefits of being fed and the indirect costs of subtracting food to relatives. As the marginal benefits of acquiring additional food decrease with decreasing levels of need, satiated offspring should be prone to favour access to food by their needy kin, thus enhancing their own indirect fitness, while concomitantly reducing costs of harsh competition with hungry broodmates. We tested this prediction in feeding trials of barn swallow (Hirundo rustica) nestlings by comparing begging behaviour and food intake of two similar-sized nestmates, one of which was food-deprived (FD). Non-food-deprived (NFD) offspring modulated begging intensity depending on their nestmate's need: when competing with FD nestmates, NFD nestlings reduced both the intensity and frequency of begging displays compared to themselves in the control trial before food deprivation. Hence, NFD nestlings reduced their competitiveness to the advantage of FD nestmates, which obtained more feedings and showed a threefold larger increase in body mass. Moderation of individual selfishness can therefore be adaptive in the presence of a needier kin, because the indirect fitness benefits of promoting its condition can outweigh the costs of forgoing being fed, and because it limits the cost of begging escalation against a vigorous competitor.     

Intraspecific female brood parasitism in the dung beetle Onthophagus taurus

Abstract.  1. Brood parasitism occurs when individuals parasitise each others' investment into parental care, and has been documented primarily as an interspecific interaction. Intraspecific brood parasitism, in contrast, is often difficult to detect and quantify, and evidence for it is comparatively scarce. The present study documents the occurrence of intraspecific brood parasitism by females of the tunnelling dung beetle Onthophagus taurus , and investigates the contributions of two variables to the propensity of female brood parasitism: female body size and dung desiccation rate.
2. Female O. taurus were found to routinely utilise brood balls made by conspecific females as food provisions for their own offspring.
3. Contrary to expectations, large and small females did not differ in the likelihood of engaging in brood-parasitic behaviour.
4. Dung desiccation rate appeared to influence likelihood of brood parasitism. Females that were given access to rapidly drying dung were significantly more likely to detect and utilise brood balls produced by conspecific females.
5. While interspecific brood parasitism has been documented in dung beetles before, the present study is among the first to present evidence for intraspecific brood parasitism as an alternative reproductive tactic of female dung beetles. Results are discussed in the context of the evolutionary ecology of onthophagine beetles.     

Analysis of genetic parentage in the tawny owl ( Strix aluco ) reveals extra-pair paternity is low

We have investigated genetic parentage in a Swiss population of tawny owls (Strix aluco). To this end, we performed genetic analysis for six polymorphic loci of 49 avian microsatellite loci tested for cross-species amplification. We found one extra-pair young out of 137 (0.7%) nestlings in 37 families (2.7%). There was no intra-specific brood parasitism. Our results are in accordance with previous findings for other raptors and owls that genetic monogamy is the rule. Female tawny owls cannot raise offspring without a substantial contribution by their mates. Hence one favoured hypothesis is that high paternal investment in reproduction selects for behaviour that prevents cuckoldry. Electronic supplementary material Supplementary material is available in the online version of this article at and is accessible for authorized users.     

Implications of multiple mating for offspring relatedness and shoaling behaviour in juvenile guppies

Polyandry (female multiple mating) can confer important benefits to females, but few studies have considered its potential costs. One such cost may arise through differences in the relatedness of offspring born to females with different mating histories; offspring born to monandrous females are always full siblings, while those produced by polyandrous females may be full or half siblings. These differences may have important consequences for social interactions among offspring. We used artificial insemination in the guppy (Poecilia reticulata), a promiscuous live-bearing fish, to evaluate shoaling behaviour in polyandrous and monandrous broods. We combined this information with known parentage data for the polyandrous broods to determine whether sibling relatedness influenced offspring shoaling behaviour. While we detected no effect of mating treatment (polyandry/monandry) on shoaling behaviour, we found that pairs of full siblings spent significantly more time shoaling (and in close proximity) than pairs of half siblings. This latter finding confirms the ability of newborn guppies to distinguish brood mates on the basis of kinship, but also suggests an important and hitherto unrealized potential cost of polyandry: a reduction in within-brood relatedness with potentially important implications for offspring social behaviour.     

Family dynamics through time: brood reduction followed by parental compensation with aggression and favouritism

Parental food allocation in birds has long been a focal point for life history and parent–offspring conflict theories. In asynchronously hatching species, parents are thought to either adjust brood size through death of marginal offspring (brood reduction), or feed the disadvantaged chicks to reduce the competitive hierarchy (parental compensation). Here, we show that parent American coots (Fulica americana) practice both strategies by switching from brood reduction to compensation across time. Late‐hatching chicks suffer higher mortality only for the first few days after hatching. Later, parents begin to exhibit parental aggression towards older chicks and each parent favours a single chick, both of which are typically the youngest of the surviving offspring. The late‐hatched survivors can equal or exceed their older siblings in size prior to independence. A mixed allocation strategy allows parents to compensate for the costs of competitive hierarchies while gaining the benefits of hatching asynchrony.     

The Evolution of Intraspecific Brood Parasitism in Birds and Insects

Many species of birds and insects engage in intraspecific brood parasitism (IBP), when a female lays eggs in the nest of a conspecific and leaves without providing parental care. These visiting females may also act to cooperate with a primary female, staying to provide parental care. Therefore, IBP and cooperative breeding can be considered extremes on a continuum of parental care provided by a secondary female. When a secondary female abandons a nest, she creates an asymmetry in parental care between herself and the host. While models of asymmetry in reproductive allocation have focused directly on relatedness between females, we lack an appropriate theoretical framework that addresses the effects of relatedness on parental care asymmetry. Here, I present an evolutionarily stable strategy (ESS) model that predicts the conditions under which IBP is favored over cooperation and solitary breeding. Intraspecific brood parasitism is less likely to evolve (relative to cooperation and solitary breeding) as the relatedness between a host and parasite increases. It can evolve, however, if parasites achieve a high overall fecundity relative to solitary females. Constraints on solitary breeding can further promote IBP under some circumstances. Cooperation is favored when relatedness is high and reproductive skew is low. This model makes several predictions regarding the conditions under which IBP may evolve, motivating a variety of experimental approaches.