Parent–offspring resource allocation in domestic pigs

Behavioural research on domestic pigs has included parent–offspring conflict, sibling competition, and the use of signals which influence resource allocation. In this paper, we review key sow–piglet behavioural studies and discuss their relevance to resource allocation theory. Sibling competition begins in the uterus and continues after birth, as piglets compete directly for access to the sow’s teats. This competition is made more severe by a unique dentition, which newborn piglets use to lacerate the faces of siblings during teat disputes. Competition often leads to the death of some littermates, especially those of low birth weight. Piglets also compete indirectly for milk, apparently by stimulating milk production at the teats that they habitually use at the expense of milk production by other teats. The complex nursing behavior of the sow appears designed to prevent the more vigorous piglets from monopolizing the milk. Sows give vocal signals which both attract piglets to suckle and synchronize their behavior during nursing episodes. Piglets give loud vocal signals when separated from the sow; calls which vary in intensity and appear to be honest signals of need. Udder massage by piglets may also serve as an honest signal of need. Parent–offspring conflict has been demonstrated experimentally in pigs. Specifically, when given the opportunity to control contact with their piglets, sows nurse less frequently, provide less milk, and lose less weight during lactation than sows that cannot control their level of contact. Because of this interesting natural history and because they are so amenable to experimentation, domestic pigs provide a rich system for testing ideas drawn from resource allocation theory. This contribution is part of the special issue “Sibling competition and cooperation in mammals” (guest editors: Robyn Hudson and Fritz Trillmich).     

Why do females have so few extra-pair offspring?

It is generally accepted that if a female can improve her offspring’s genetics via extra-pair copulations (EPC), it is by copulating with extra-pair males whose phenotypes are more superior or whose genes are more compatible to hers than those of her bonded male. Here, we present a model that puts together uncertainties about the male genetic quality, a postcopulatory sperm bias in favor of the better or the more compatible genes, and costs that females pay by being choosy about extra-pair male quality. The model’s conclusions challenge traditional views of good genes explanations of EPC. When phenotypes give incomplete information about genotypes, a female choosing a phenotypically superior extra-pair male, may nevertheless find herself trading good genes of a bonded male for poor genes of an extra-pair male. Such “unfortunate sperm replacements” can limit the female involvement in EPC even when EPC are otherwise cost-free. The model also shows that even a female bonded to a phenotypically superior male may benefit by EPC, provided that sperm competition is biased toward sperm with more fit or more compatible genes. Furthermore, if choosiness is sufficiently costly, a female may even do best by copulating with a random extra-pair male.     

Individual recognition and potential recognition errors in parent–offspring communication

The recognition of food-provisioning parents is crucial for fledglings of many bird species. Vocalizations are the most commonly used cues in avian parent–offspring communication, and it has been shown in several species that fledglings respond specifically to their parents' contact calls. However, fledglings occasionally also react to unrelated adults. Such responses may reflect recognition errors or alternatively a strategy of fledglings to obtain food or other direct benefits from unrelated adult birds. In a playback experiment, we tested whether zebra finch Taeniopygia guttata fledglings perceive variation in adult call signatures to recognize their parents and whether the propensity to respond to unrelated individuals is related to the gender of adults and to signal properties of male and female calls. Male calls are learnt and show high intra-sexual variation, which may improve the accurate recognition of the father's individual signature. In contrast, calls of adult females are innate, show lower intra-sexual variation such that the mother's call is more likely to be confused with another female call. We demonstrate that fledglings are able to recognize their parents. In addition, fledglings reacted more strongly to unrelated females compared with unrelated males. Our findings suggest that responses to unrelated adults may reflect recognition errors and indicate the importance of variation in identity signals for individual recognition processes in parent–offspring communication.     

Predation of calanoid copepods on their own and other copepods’ offspring

Predation of eggs and nauplii by adult copepods is often used to explain unexpected death rates in population dynamics studies, but the phenomenon has been rarely investigated or quantified. Therefore, we studied the predatory feeding of adult females (Acartia clausi, Centropages hamatus, Centropages typicus, and Temora longicornis) on their own and other species’ eggs and young nauplii with different densities of single animal-prey, mixtures of animal-prey and in the presence of diatoms. All species preyed on eggs and nauplii of their own and all other species. Maximal egg predation varied between 7 and 64 eggs fem^?1 day^?1. Ingestion of Centropages spp. eggs was lowest, potentially due to the spiny egg surface. Maximal feeding rates on nauplii ranged from 5 to 45 nauplii fem^?1 day^?1. T. longicornis preferred eggs, when eggs and nauplii were offered together at the same densities, and the other predators selected for nauplii. At a diatom concentration of 60 μg C l^?1 predation on eggs by C. typicus was higher than without algae, whereas A. clausi and T. longicornis did not change their uptake of eggs. Feeding on nauplii in the presence of diatoms was again enhanced in C. typicus, and unaffected in A. clausi and C. hamatus. T. longicornis reduced its feeding on nauplii in the presence of diatoms. Calculated predation rates, using field abundances of predators and prey, suggest that predation of copepods on their own young stages may account for ca. 30 % of total mortality of young stages in North Sea copepod populations.     

Parental investment without kin recognition: simple conditional rules for parent–offspring behavior

Species differ widely with regard to parental investment strategies and mechanisms underlying those strategies. The passing of benefits to likely genetic offspring can be mediated through a number of different computational and behavioral systems. We report results from an agent-based model in which offspring maintain proximity with parents and parents transmit benefits to offspring without the capacity of either parent or offspring to “recognize” one another. Instead, parents follow a simple rule to emit benefits after reproducing and offspring follow a simple rule of moving in the direction of positive benefit gradients. This model differs from previous models of spatial kin-based altruism in that individuals are modeled as having different behavioral rules at different life stages and benefits are transmitted unidirectionally from parents to offspring. High rates of correctly directed parental investment occur when mobility and sociality are low and parental investment occurs over a short period of time. We suggest that strategies based on recognition and bonding/attachment might serve to increase rates of correctly directed parental investment under parameters that are shown here to otherwise lead to high rates of misdirected and wasted parental investment.     

Does the African social spider Stegodyphus dumicola control the sex of individual offspring?

By scoring the chromosome number of developing embryos, we show that the sex ratio bias of the African social spider Stegodyphus dumicola Pocock is the result of an overproduction of female embryos. Only 17% of 585 embryos sexed from 14 egg sacs were male, a significant departure from a 1:1 sex ratio. We also explored the possibility of direct control of the sex of individual offspring in this species by examining the variance in the number of males per sac and the spatial distribution of male and female embryos within the sacs. We postulated that a variance in the number of males per sac lower than binomial (i.e., underdispersed or precise sex ratios) or a non-random distribution of male embryos within the sacs would suggest direct control of the sex of individual offspring. We found that the variance in the number of males per sac was indistinguishable from binomial and significantly larger than expected under exact ratios. Likewise, the spatial distribution of male embryos within three sacs examined was no more clustered than expected by chance. The sex ratio biasing mechanism in this species, therefore, apparently only allows control of the mean sex ratio but not of its variance. We present randomization and Monte Carlo methods that can be applied to test for departures from a random spatial arrangement of male and female embryos in an egg mass and for departures from binomial or exact ratios when not all members of a clutch have been sexed. Received: 21 October 1998 / Received in revised form: 23 March 1999 / Accepted: 26 April 1999     

Active protection of unrelated offspring against parasitoids. A byproduct of self defense?

Natural enemies exert selection pressure on their prey. Predators and parasitoids drive their prey into the evolution of novel traits to cope with this stress. When eggs and juveniles are the target of enemies, defense strategies may rely on adults. However, it is not easy to predict whether adults should actively protect unrelated offspring. Females of the golden egg bug (Phyllomorpha laciniata) mainly oviposit on conspecifics of either sex. Females can also lay eggs on their food plant. Eggs placed on plants suffer from a higher mortality caused by natural enemies than eggs carried by bugs. Females never carry their own eggs and males are seldom related to the eggs they carry. We experimentally explored if conspecifics protect the eggs by studying the behavioral interaction between P. laciniata individuals and the specialist egg parasitoid Gryon bolivari. All bugs exhibited active responses against parasitoids regardless of the sex of the bug, the egg load, and their mating status. Most of the responses prevented parasitoids from reaching the eggs, and thus they reduced the risk of egg parasitization. Although responses of bugs were effective to overcome parasitoid attacks, we suggest that egg protection against parasitoids has evolved as a co-opted trait from a general defense of adult bugs against enemies. In this system, egg defense is not an individual's strategy to protect the offspring, but rather a consequence of the eggs being attached to one's body. It may also explain the low parasitization carried eggs suffer in the wild. The results further highlight the idea of conspecifics as an enemy-free space in P. laciniata.     

Parent–offspring dietary segregation of Cory’s shearwaters breeding in contrasting environments

In pelagic seabirds, who often explore distant food resources, information is usually scarce on the level of trophic segregation between parents and their offspring. To investigate this issue, we used GPS tracking, stable isotopes and dietary information of Cory’s shearwaters Calonectris diomedea breeding in contrasting environments. Foraging trips at Selvagem Grande (an oceanic island) mainly targeted the distant African coast, while at Berlenga island (located on the continental shelf), shearwaters foraged mainly over nearby shelf waters. The degree of isotopic segregation between adults and chicks, based on δ¹³C, differed markedly between the two sites, indicating that adult birds at Selvagem fed their chicks with a mixture of shelf and offshore pelagic prey but assimilated more prey captured on coastal shelf waters. Isotopic differences between age classes at Berlenga were much smaller and may have resulted from limited dietary segregation or from age-related metabolic differences. The diet of shearwaters was also very different between the two colonies, with offshore pelagic prey only being detected at Selvagem Grande. Our findings suggest that spatial foraging constraints influence resource partitioning between pelagic seabirds and their offspring and can lead to a parent–offspring dietary segregation.     

Parent–offspring and sibling conflict in Galápagos fur seals and sea lions

Parent–offspring conflict theory is well supported by theoretical arguments. However, empirical observations are often difficult to interpret and have contradicted one of its most appealing predictions that parent and offspring should disagree over killing of nest or littermates. We present the first examples of deadly conflict between siblings of different cohorts. In Galápagos fur seals (Arctocephalus galapagoensis) and sea lions (Zalophus wollebaeki), mothers often wean their single offspring at 2 years. This leads to a situation where up to 23% of all pups are born while the older sibling is still being nursed. Younger siblings are disadvantaged by being born lighter than neonates without older still dependent siblings. Pups born while an older sib is still dependent grow less in early life (fur seal) and suffer increased early mortality (both species) through direct aggression or scramble competition with the older sibling. This effect is much stronger in years of high sea surface temperature (El Niño) indicating low marine productivity and if the older offspring is a male. In both species, mothers interfere aggressively in this conflict by defending the younger offspring. In years of El Niño, intense resistance to maternal aggression by the older offspring happens frequently in the fur seal. Such resistance against weaning can induce maternal neglect of the newborn. Given substantial year to year variation in offspring growth, maternal aggression forces weaning in the older sibling only if it has reached sufficient size to support itself by foraging. In Galápagos fur seals, pups with older siblings can either represent insurance against loss of older offspring or extra reproductive value.     

Does the cost of polygyny in house wrens include reduced male assistance in defending offspring?

Summary This study investigated whether reduced male aid in defending offspring potentially reduces the fitness of females choosing already-mated males in the house wren (Troglodytes aedon), a small, territorial songbird. Frozen snakes were placed at 23 nests of monogamously mated males and 12 secondary nests of bigamously mated males. All presentations were made during incubation stages of females attending focal nests. Snakes were placed at nests of secondary females when nests of their primary counterparts contained young 5–9 days old. Males are most attentive to primary nests during this period and should therefore be relatively inattentive to secondary mates and nests. Nevertheless, an equal proportion of monogamous and bigamous males discovered snakes within 15 min, and mean time to discovery, when discovery occurred, did not differ with nest status. Monogamous and bigamous males were also equally likely to attack snakes physically once discovered. Monogamous males appeared no more likely to discover snakes than bigamous males for two main reasons. First, although monogamous males were near focal nests (i.e., < 10 m) more often than bigamous males, monogamous males tended to stay out of view of nests for long periods. In contrast, bigamous males always went immediately to focal nests upon arriving in their vicinity. Second, about one-third of monogamous males in this study spent much of their time during trials at the far edges of their territories advertising for secondary mates. Our experiment suggests that reduced male aid in defending nests against small, diurnal predators probably does not contribute to the cost of polygyny in house wrens. Correspondence to: L.S. Johnson     

On the coadaptation of offspring begging and parental supply—a within-individual approach across life stages

Parental care is often characterized by complex behavioral interactions between offspring soliciting for food and parents providing food. During this interplay both behaviors, offspring begging and parental provisioning, can exert a selective pressure on the expression of the other. It has, therefore, been predicted that traits involved in this interplay may coevolve and ultimately become (genetically) correlated. Such covariation has—at least at the phenotypic level—been found in a number of cross-fostering studies, including evidence from the canary (Serinus canaria), our model species. However, a common challenge for these studies has been to establish a genetic covariation given the difficulty to disentangle the relative contribution of genetic and maternal effects, as the latter may act already before cross-fostering. We addressed this problem by studying within-individual covariation between begging (expressed at the nestling stage) and provisioning (expressed at the adult stage). In addition, we estimated the degree of heritability of these behaviors using parent-offspring regressions, as inheritance forms a prerequisite for any genetic correlation. Both traits showed a low to moderate non-significant heritability, similar to those previously reported in other bird species. However, offspring begging and parental provisioning did not covary at the intra-individual level. Thus, individuals begging intensively as nestlings were not necessarily individuals that provided more food as adults or vice versa. These findings provide important insights for our understanding of coadaptation, suggesting that factors other than genes such as maternal effects may play a role in adjusting offspring begging to the levels of parental provisioning.     

Prey size increases with nestling age: are provisioning parents programmed or responding to cues from offspring?

As offspring grow, parents often feed them with different sizes or taxa of prey to suit the changing nutritional or energetic demands. We investigated whether such changes in prey types were innate and inflexible or whether they were based on the proximate cue of offspring size. We created experimental broods in which parent blue tits Cyanistes caeruleus and pied flycatchers Ficedula hypoleuca received either older nestlings simulating rapid development or younger nestlings simulating delayed development. The size of prey increased over time in all brood types, suggesting a strong programmed pattern of foraging by parents. However, delayed broods were provisioned with smaller prey than control or advanced broods indicating some plasticity in the response by the parents to the size of nestlings. Although female birds brought smaller prey than male birds, both sexes showed the same rate of increase of prey size with time and brought similar types of prey items. The proportion of soft, digestible larva prey in the nestling diet decreased over time in pied flycatchers but increased in blue tits. Counter to the hypothesis that spiders provide unique and preferred nutrients for young nestlings, the proportion of arachnids in the diet did not change with nestling age for either species. The lack of treatment effect on the taxa of prey delivered suggests that temporal shifts in diet composition are not driven by the proximate cues of nestling age or size but that the feeding patterns are fairly innate and fixed in these altricial birds.