Kin recognition by juvenile predatory mites: prior association or phenotype matching?

Kin recognition, the biased treatment of conspecific individuals based on genetic relatedness, is a widespread phenomenon in animals. The most common mechanisms mediating kin recognition are prior association (familiarity) and phenotype matching. Recognition based on prior association allows identifying familiar individuals. Recognition based on phenotype matching is an extension of prior-association-based recognition and allows identifying familiar and unfamiliar individuals due to a shared phenotypic trait. I investigated which of the two mechanisms is used by cannibalistic juvenile predatory mites, Phytoseiulus persimilis. Protonymphs that were associated with either siblings or non-kin discriminated familiar and unfamiliar larvae and preferentially cannibalized the latter irrespective of genetic relatedness. In contrast, despite previous association with either siblings or non-kin, protonymphs did not discriminate unfamiliar sibling and unfamiliar non-kin larvae. Association in the larval stage therefore mediated kin recognition based on familiarity, but not phenotype matching in cannibalistic P. persimilis protonymphs. Furthermore, in the presence of a familiar prey individual, sibling cannibalism occurred significantly sooner than non-kin cannibalism. This quick sibling cannibalism may have been the consequence of preferential association of siblings and/or may indicate the occurrence of an alternative cannibal phenotype. I discuss the adaptive significance of prior-association-based recognition for P. persimilis juveniles and emphasize the ability of P. persimilis to use multiple recognition mechanisms in dependence of the ontogeny and the ecological context.     

Kin recognition in the common lizard

The ability to recognize parents has never been reported in species in which parents do not provide care to their young; in such species, only sibling recognition has been found. However, there may be several advantages of parent recognition, even in the absence of parental care. We investigated the ability of neonates to recognize olfactory cues from both their mother and siblings in the common lizard, Lacerta vivipara, a species without parental care. Juveniles from 264 gravid females were reared for 2 days either with their mother, with another female, or separated from all other adults. Juveniles from some families were split into two or three groups so that each juvenile was unfamiliar with a subset of its siblings. After 2 days, we offered the juveniles a choice of two nocturnal shelters: one containing a lizard odor and the other without odor. The response to the odor of an unrelated and unfamiliar adult was influenced by both the sex of the adult and the sex of the juvenile. Juveniles of both sexes recognized the odor of their mother whether they were familiar with her or not (pre-natal determinism). Juveniles recognized familiar but not unfamiliar siblings (post-natal determinism). In the wild, spatial association with kin declines shortly after birth. Thus, recognition of the mother is likely to have biological relevance. Recognition of the mother may reduce competition and/or enhance juvenile establishment. Received: 15 May 1997 / Accepted after revision: 29 December 1997     

Shoaling decisions in three-spined sticklebacks (<Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis>)—familiarity,kinship and inbreeding

Shoaling with familiar kin is a well-known phenomenon. It has been described both for adult and for fry of three-spined sticklebacks (Gasterosteus aculeatus). However, evidence of preference for kin independent of familiarity is scarce. Furthermore, inbreeding effects have not been studied for shoaling preferences and there is a lack of studies about changes in individuals’ ability to recognise kin during different phases of life history. We gave inbred and outbred, nonreproductive sticklebacks of different age the choice to shoal with a group of familiar siblings vs unfamiliar non-siblings and with unfamiliar siblings vs unfamiliar non-siblings. Subadult sticklebacks preferred to shoal with familiar kin over unfamiliar non-kin, but inbred and outbred individuals had similar preferences. When given the choice between unfamiliar siblings and unfamiliar non-sibs, adult outbred fish preferred the shoal of kin, while inbred fish behaved indifferently. Body characteristics of the group such as body mass, standard length and condition of its members did not significantly explain the shoaling preferences for kin. Thus, sticklebacks were capable of recognising familiar and unfamiliar kin. The latter capability was lost by inbreeding.     

A field test of the effects of familiarity and relatedness on social associations and reproduction in prairie voles

Inbreeding depression is a well-documented phenomenon. In animals, one means of avoiding the costs of inbreeding is through the recognition and avoidance of kin as mates. Prairie voles (Microtus ochrogaster) are short-lived, socially monogamous rodents that demonstrate inbreeding depression in the laboratory. Field data indicate that pair formation in nature is opportunistic but pairing among close relatives seems uncommon. We examined the role of relatedness and familiarity on prairie vole social associations and reproduction by placing adult voles into 0.1-ha enclosures with familiar siblings, unfamiliar siblings, and unrelated, unfamiliar conspecifics. Live-trapping data indicated that indices of social pair bonding were random with respect to relatedness and familiarity. Among females whose litters were sired by a single male, litters were significantly more likely to be sired by unfamiliar than familiar males, but the number of litters sired by males that were unrelated to their partner was not different from the number of litters sired by males that were related to their partner. Additionally, females that produced offspring with familiar siblings were significantly more likely to have litters with multiple paternity than females not producing offspring with familiar siblings. However, multiple paternity was not influenced by relatedness of sires. Finally, older individuals were more likely to produce offspring with each other than with younger individuals. Our findings suggest that prior association is a more important mechanism of inbreeding avoidance than phenotype matching for prairie voles mating under ecologically relevant conditions.     

Effects of kinship on growth of a live-bearing reef fish

The influence of genetic relatedness on the individual performance (e.g. growth, development) of animals is often tied to agonistic or cooperative behaviors among conspecifics, and studies of the effects of kinship have produced mixed results. To explore genetic relatedness independent of these behaviors, we investigated the effects of kinship on the growth of the kelp perch Brachyistius frenatus, a live-bearing, planktivorous marine reef fish that is capable of only limited dispersal. Although juveniles occur in aggregations and compete for food resources, they do not exhibit overt aggressive or cooperative behavioral interactions. We hypothesized that under competition and in the absence of these behaviors, sibling and non-sibling groups of juvenile B. frenatus raised at the same densities in the field would not differ in average growth, but that siblings would exhibit lower variation in growth, simply due to genetic similarities in inherent growth rates. Pregnant, female kelp perch were collected and placed in cages until parturition was complete. Groups of young, recently born from the same mother or from different mothers, were then raised in the field for 9 wk. Our results revealed that average growth rates were similar between sibling and non-sibling treatments. While variation in growth increased initially in non-siblings, siblings showed little such variation. This divergence, however, was not consistent over the duration of the experiment, and variation in the growth of siblings ultimately converged with that of non-siblings. Effects of genetic relatedness would be most likely to manifest themselves early after birth, before environmental factors exert their influence, and this may explain the initial separation but eventual convergence in variation in growth between sibling and non-sibling treatments. For B. frenatus and other organisms that will encounter relatives and compete for resources without overt behavioral interactions, the degree of kinship may play a minor role in the demography of local populations. Received: 26 January 1998 / Accepted: 30 September 1998     

Costs of switching social groups for dominant and subordinate dark-eyed juncos (Junco hyemalis)

I quantified the costs of switching from a familiar to an unfamiliar flock for captive dark-eyed juncos (Junco h. hyemalis) by measuring several physiological and behavioral variables before and after flock switching. Birds that were initially dominant dropped in status in unfamiliar flocks, and experienced increased metabolic rates, while subordinate birds appeared to undergo less physiological change when switching flocks. This difference occurred despite a lack of any rank-related differences in the effects of joining a new flock on rates of aggression, weight change, access to food, or plasma corticosterone levels. These results suggest that for dominant, but not subordinate, individuals there is a measurable metabolic cost to joining a new social group, even in the absence of adverse factors such as food limitation. Dominant individuals may be less likely than subordinates to leave familiar flocks because of their higher metabolic costs when joining a new social group.     

Incest avoidance and bonding between siblings in gerbils

Summary Social and sexual preferences for siblings versus non-siblings have been investigated in Mongolian gerbils (Meriones unguiculatus) in a series of laboratory and outdoor enclosure (100 m²) studies. When first social contact took place at pairing in adulthood full siblings and nonsiblings did not differ with respect to onset of reproduction. Correspondingly, both siblings and non-siblings paired at weaning age had a delayed onset of reproduction. Thus, no effect could be established in either case, related to the individuals' relatedness, but the importance of social exposure was clear. Non-siblings paired when 2 months old had a delayed onset of reproduction, which did not differ statistically from the onset in siblings, raised together, and housed pairwise since the same age. When sexually mature animals were paired at 3 months of age, siblings were found to start reproducing later than non-siblings (Ågren 1981). Following an initial delay in both siblings and nonsiblings paired when 5 months old, all non-sibling pairs reproduced before any sibling pair. At pair formation, at least the females in both groups were known to be sexually immature. These results indicate that for sibling-bonding to occur social exposure may be delayed until the animals are old enough, or somatically developed, to mature sexually. Thus, social exposure before weaning age during the period for primary socialization seem not to be crucial, nor the actual maturational state, sexually, in older females. To study the stability of the social bonds between siblings and non-siblings, animals kept pairwise in the laboratory were released in large outdoor enclosures. Pairs brought together before the age of sexual maturity did not remain stable, whether or not the former cagemates were siblings. Non-sibling pairs formed after this age, which had also reproduced successfully in the laboratory, did remain stable. Social and sexual interactions were studied within and between two mixed-sex sibling groups of four. The sibling groups had the possibility to establish group territories before being exposed to each other. Although the sibling groups remained stable, the females still preferred non-sibling males as sexual partners. However, socially dominant brothers copulated more frequently than subordinant brothers. This rank difference was not evident in non-siblings.     

Chemical rival recognition decreases aggression levels in male Iberian wall lizards, <Emphasis Type="Italic">Podarcis hispanica</Emphasis>

In an agonistic interaction, the assessment of the probable outcome of future encounters with the same individuals may be the best way of decreasing costs of fighting, but this may only be accomplished if animals are able to recognize individual conspecifics. We staged encounters between male lizards, Podarcis hispanica, to examine whether odoriferous cues are involved in rival recognition during agonistic interactions. We experimentally manipulated the odour of intruding males, creating familiar males with their own odour or bearing odours of unfamiliar males, and unfamiliar males bearing unfamiliar odours or odours of familiar males. The results showed that when familiar males were impregnated with scents from unfamiliar males, they elicited an aggressive response by resident unmanipulated males similar to that observed for a new unfamiliar male with unfamiliar odour. This suggests that resident males were unable to recognize familiar males when their own scents were removed. In contrast, responding males were less aggressive towards familiar males impregnated with their own odour and towards unfamiliar males impregnated with scents of familiar males, suggesting that when two males have already interacted, their scents become familiar for both males, and that the detection in successive encounters of the familiar scent suffices to reduce the aggressive response of territorial males. Therefore, recognition mechanisms based on chemical cues during agonistic encounters may contribute to reducing the intensity and the costs of fighting in P. hispanica and may play an important role in the organization of their social system.     

Familiarity with adults,but not relatedness,affects the growth of juvenile red-backed salamanders (<Emphasis Type="Italic">Plethodon cinereus</Emphasis>)

The relative roles of kinship and familiarity in affecting an individual’s growth and fitness are not easy to disentangle. Not only is an individual more likely to have prior behavioral interactions with conspecifics in close proximity, it may also be related (in terms of kinship) to those nearby conspecifics. While some studies have inferred that kin discrimination affects fitness correlates, other studies found that familiarity alone can reduce aggressive interactions, thus increasing fitness. These studies have all focused on intra-age class pairs or groups. However, many animals interact with conspecifics from different cohorts. In many populations, adults of Plethodon cinereus territorially defend rocks and logs that retain moisture and food resources. We investigated whether juveniles of P. cinereus grew more in the presence of adults that were relatives or familiar. We collected pairs of juveniles and adults found under the same cover objects in the forest (familiar) and pairs of juveniles and adults found under different cover objects, approximately 10 m apart (unfamiliar). We determined parentage and relatedness of the adult–juvenile pairs and then placed these pairs in semi-natural mesocosms for 17 days. We found that juveniles housed with familiar adults had significantly greater increases in mass and snout–vent length than juveniles housed with unfamiliar adults in 2006 but not in 2007. Relatedness had no effect on growth. In addition, juveniles cohabitating with adults were not more likely to be their offspring. At least under certain environmental conditions, familiarity with adults, independent of relatedness or parentage, increased the growth of juvenile salamanders.     

Evidence of kin-selected tolerance by nestlings in a siblicidal bird

Behaviorally dominant members of blue-footed booby (Sula nebouxii) broods can effect siblicide by restricting access of subordinate siblings to parents providing food. In spite of their capacity for siblicide, dominant chicks permit subordinates to feed during short-term food shortage; in fact, the proportion of the food that the dominant takes is independent of the total amount delivered in older chicks. A model of optimal food distribution suggests that dominant chicks maximize their inclusive fitness with this pattern, rather than by satisfying their own food requirements and leaving what remains for the subordinate sibling. The indirect reproductive potential represented by a chick's sibling appears to have influenced the evolution of siblicidal brood reduction in this species.     

How does salinity tolerance influence the distributions of <Emphasis Type="Italic">Brachionus plicatilis</Emphasis> sibling species?

Environmental salinity is important in defining Brachionus plicatilis sibling species distributions. However, while salinity influences distributions, sibling species often co-exist. Three different mechanisms potentially account for the partial co-occurrence of sibling species: (1) siblings have differing salinity tolerances that partially overlap; (2) siblings physiological tolerances may be commonly broad, but relatively small differences in tolerances differentiate distributions via interactions e.g. competition; or (3) siblings distributions may be influenced by physical factors other than salinity. Here, we assess the extent of salinity tolerance in three B. plicatilis sibling species (B. plicatilis 6TUR, B. plicatilis IOM and B. rotundiformis 6TOS) by measuring population growth rate (μ, day⁻¹) and egg development time in response to salinity (5–60‰) and salinity fluctuations (≤ Δ40‰). Sibling species were identified by analysis of the mitochondrial COI gene, and salinity responses were compared by regression analysis. Responses differed significantly between siblings, although the broad trends were similar. Positive growth occurred at all salinities, and highest growth rates ranged between 0.93 and 1.08 day⁻¹ at 16–18‰. Rapid changes in salinity reduced growth rates, but net mortality occurred only in one treatment (100% mortality on transfer from 10 to 40‰). Egg development time was largely invariant with salinity except for B. plicatilis IOM and where rotifers were transferred from 30 to 60‰. We indicate that several siblings are similarly euryhaline and tolerate salinity fluctuations. Undoubtedly, wide tolerances in B. plicatilis are adaptations to ephemeral and seasonally variable habitats. Given common broad salinity tolerances, it is unlikely that the differential distributions of sibling species are a direct result of physiological constraints. Instead, we illustrate using a simple model that subtle differences in physiological tolerances may have important impacts on interactions between sibling species, which may in turn influence distributions.     

Sibling recognition in spiny mice (Acomys cahirinus)

Summary Sibling recognition by spiny mice (Acomys cahirinus) was investigated by housing groups consisting of two pairs of littermates together and recording frequency of dyadic pairing. A total of 136 animals (68 pairs of siblings) were tested in three experiments. Sibling pairs were observed more often than pairings between nonsiblings; however, such preferences were no longer evident if the nonsiblings were exposed to one another prior to testing. Animals made anosmic through zinc sulfate treatment did not differ on their frequencies of sibling vs. nonsibling pairing and showed a higher incidence of group huddling (by all four animals) than did intact controls. Weanling A. cahirinus appear to be able to recognize (i.e., are attracted to) their littermate siblings through olfactory cues, which seems to be a modifiable attraction to odors to which the littermates were exposed rather than an irreversible imprinting-like process.The research project reported herein was supported by grant # 00973 from NICHD     

Further experiments on olfactory navigation and non-olfactory pilotage by homing pigeons

Summary Supplementary to a previous investigation (Wallraff and Neumann 1989), further experiments were conducted with homing pigeons that were either familiar of unfamiliar with the release area, and that had or lacked olfactory access to environmental odours. All four possible pairwise combinations of these factors were tested. The previous results were confirmed, showing that in an unfamiliar area olfactory inputs are necessary for home-related orientation, while in a familiar area both olfactory and non-olfactory information can be utilized and each is more or less redundant as long as the other kind of information is also available. The degree of redundancy of olfactory inputs varies, obviously depending on the pattern of individual local experience. Correspondence to: H.G. Wallraff     

Heart rate changes reveal that little blue penguin chicks (Eudyptula minor) can use vocal signatures to discriminate familiar from unfamiliar chicks

Researchers investigating social recognition typically measure only behavioural responses during discrimination tests - physiological changes have been largely ignored. We examined whether little blue penguin chicks (Eudyptula minor) could distinguish siblings from other chicks using auditory cues, by measuring behavioural and heart rate changes during playback experiments. Chicks were exposed to five treatments: the begging calls of siblings, neighbouring chicks and unfamiliar chicks, and two controls (heterospecific begging calls and music). We also determined if chicks developed distinctive begging calls, by using F-ratios to quantify inter- versus intra-individual variability in a range of acoustic parameters, and applying a discriminant-function analysis. Inter-individual variation was greater for pitch than for temporal or amplitude parameters, suggesting that call pitch may be important for individual recognition. The discriminant-function analysis showed each chick's calls were distinctive and could act as a vocal signature. Treatments did not instigate different behavioural responses. However, chick heart rates during playback of sibling calls were significantly higher than those recorded during stranger, but not neighbour, playback. A simple recognition system based on familiarity may allow this plesiomorphic and loosely colonial penguin to gain at least some of the benefits associated with more advanced sibling recognition systems (some highly colonial seabirds discriminate siblings from neighbouring chicks). Heart rate could be a useful measure of social recognition abilities, particularly in species where changes in behaviour are not always evident or are difficult to observe.     

The effects of mating on infanticide and pup discrimination in white-footed mice

Summary A laboratory study was conducted with white-footed mice (Peromyscus leucopus) to determine (1) if cohabitation and/or successful mating inhibits infanticide, and if so for how long, and (2) if males and females can discriminate between their own (familiar) and strange (unfamiliar) pups. Infanticidal males and females that were paired for 15 days and did not reproduce were not inhibited from killing pups, whereas infanticidal males and females that were paired until they reproduced were inhibited from committing infanticide at 4 days postpartum. Neither males nor females discriminated between familiar and unfamiliar pups with regard to engaging in infanticide. Approximately 50% of wild-caught males and females killed pups in the laboratory. Infanticidal pairs bred significantly sooner than did noninfanticidal pairs. The results are consistent with the promiscuous nature of P. leucopus males and territoriality of P. leucopus females. Offprint requests to: Donna M. Cicirello, Kellogg Biological Station, 3700 E. Gull Lake Drive, Hickory Corners, MI 49060, USA     

Individual and species recognition in centrarchid fishes: evidence and hypotheses

Summary We conducted laboratory experiments to determine if juveniles of three species of centrarchid fishes displayed abilities for species or individual recognition. In one experiment we reared rock bass (Ambloplites rupestris) in social isolation and in social groups. Both the isolated and group-reared fish spent significantly more time close to conspecifics than to heterospecifics. These results suggest that species recognition in rock bass is controlled by a closed genetic program and that social experience is not necessary. A second set of experiments was conducted to determine if year-old blue-gill (Lepomis macrochirus), pumpkinseed (L. gibbosus), and rock bass juveniles could discriminate between familiar and unfamiliar conspecifics. Bluegill spent significantly more time with familiar conspecifics than with unfamiliar conspecifics, while the other two species displayed no such trend. Bluegill spent significantly more time with familiar conspecifics than did either of the other two species. We postulate that these interspecific differences in recognition abilities may be related to differences in habitat and group parameters among the species.     

Binary individual recognition in hermit crabs

One mechanism that permits the maintenance of dominance hierarchies is individual recognition, defined as the ability of an animal to recognize a conspecific on the basis of one or more identifying cues, and to associate it with experiences of victories or defeats that the animal has gained from preceding encounters with that particular individual. We examined whether the long-clawed hermit crab, Pagurus longicarpus, could differentiate between unfamiliar and familiar opponents. The experimental protocol was designed to control in pairs of interacting individuals several factors together, such as status and relative size of the opponent, as well as species, quality, and fit of the inhabited shell. The hermit crabs were more reactive and their agonistic level was higher in unfamiliar than in familiar pairs; in addition, betas were more prone to initiate an interaction with unfamiliar than with familiar alphas. The alternative explanation—that the ability to discriminate between familiar and novel shells can explain our results per se— was tested following, in part, Jackson and Elwoods (1989) protocol for Pagurus bernhardus and was, at least for this species, rejected. This study did not determine whether a true individual recognition occurs, but demonstrated that P. longicarpus categorizes the individuals into two heterogeneous subgroups, thus being capable of a binary discrimination among opponents.Communicated by T. Czeschlik     

Discrimination of different social companions in spectacled parrotlets (Forpus conspicillatus): evidence for individual vocal recognition

Individual recognition is generally assumed to be a prerequisite for establishing and maintaining a complex social system. Indeed, there is good evidence that highly social species have complex systems of vocal communication with individual recognition by acoustic cues. In this study, we provide experimental evidence that vocal class and individual recognition is present in a non-passerine bird, the spectacled parrotlet (Forpus conspicillatus). Spectacled parrotlets live in a complex system of social relationships. Soon after fledging, the young establish close sibling relationships which are important for successful socialization, pairing and reproduction. In a series of playback experiments we tested if spectacled parrotlets use contact calls for vocal recognition. The results showed that spectacled parrotlets discriminate between the contact calls of different social categories. Adult birds preferred to respond to the contact calls of their mates. Subadult individuals recognized the contact calls of their siblings. During the period of pair bond formation, the affiliative contacts to the siblings decrease, but the parrotlets continue to respond to the calls of their siblings. This is the first evidence that vocal sibling recognition might outlast the period of strong sibling interaction and extends into the period of pair bond formation. In cases of mate loss or divorce, the acoustic contact to their siblings might facilitate the re-establishment of close sibling relationships. Received: 29 October 1997 / Accepted after revision: 5 April 1998     

Boldness and body size of male Spanish terrapins affect their responses to chemical cues of familiar and unfamiliar males

Recognition and avoidance of conspecifics based on chemical cues could reduce the risk of aggressive interactions between males. Success in agonistics encounters with unfamiliar males should be lower than with previously known familiar males. Then, males should avoid the chemicals from unfamiliar males with respect to those from familiar males. However, boldness and size could affect the outcome of encounters between males and, consequently, the response to chemical cues of conspecific males. We compared the time spent by male turtles Mauremys leprosa in water pools with chemical stimuli from unfamiliar or familiar males or with their own chemical stimuli. We also performed a behavioral test to estimate boldness of turtles in an antipredatory situation. Turtles avoided the chemicals from unfamiliar males respect to familiar ones and their own odors, but their responses depended on boldness and size of the tested turtle. Bold turtles avoided water with chemicals of unfamiliar males, but not with chemicals of familiar males, whereas shy turtles avoided chemicals of both familiar and unfamiliar males. On the other hand, large males avoided the odor from unfamiliar males, but small males did not avoid water with the odor from other males. Results suggest that male M. leprosa can detect chemicals released to water from conspecific males and discriminate between familiar and unfamiliar males. However, responses to these chemicals depended on boldness and body size of the responding turtle because these factors may affect intrasexual competition.     

Hunger and food allocation among nestlings of facultatively siblicidal ospreys

Summary Previous studies of food allocation among nestlings of siblicidal birds have focussed on the proximate link between food and aggression. However, food sharing among sibs (and brood reduction) need not involve aggression. Here I examine the role of hunger (defined operationally in terms of the amount of food eaten recently) within the broader framework of passive and aggressive food-sharing among nestlings of facultatively siblicidal ospreys (Pandion haliaetus). Feeding among brood members was hierarchical; senior, dominant sibs ate more when hungry, leaving a smaller residual share of food for junior sibs. Senior sibs did not become more generous at large meals (i.e., the prospect of a large meal did not quell the selfish tendencies of senior sibs). That individuals ate more when hungry indicates a proximate link between food and the allocation of resources among siblings. Overall, aggression was infrequent and seemed to be used when junior sibs contested food allocation at meals. Aggression was diminished and food allocation was skewed toward the junior sib in broods with artificially exaggerated hatching intervals, suggesting that senior sibs were more generous when their dominant status was not threatened.Offprint requests to the present address