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.     

A test of reproductive skew models in a field population of a multiple-queen ant

Determining the evolutionary basis of variation in reproductive skew (degree of sharing of reproduction among coexisting individuals) is an important task both because skew varies widely across social taxa and because testing models of skew evolution permits tests of kin selection theory. Using parentage analyses based on microsatellite markers, we measured skew among female eggs (n=32.3 eggs per colony, range=20–68) in 17 polygynous colonies from a UK field population of the ant Leptothorax acervorum. We used skew among eggs as our principal measure of skew because of the high degree of queen turnover in the study population. Queens within colonies did not make significantly unequal contributions to queen and worker adult or pupal offspring, indicating that skew among female eggs reflected skew among daughter queens. On average, both skew among female eggs (measured by the B index) and queen–queen relatedness proved to be low (means±SE=0.06±0.02 and 0.28±0.08, respectively). However, contrary to current skew models, there was no significant association of skew with either relatedness or worker number (used as a measure of productivity). In L. acervorum, predictions of the concession model of skew may hold between but not within populations because queens are unable to assess their relatedness to other queens within colonies. Additional phenomena that may help maintain low skew in the study population include indiscriminate infanticide in the form of egg cannibalism and split sex ratios that penalize reproductive monopoly by single queens within polygynous colonies.     

Kinship and food availability influence cannibalism tendency in early-instar wolf spiders (Araneae: Lycosidae)

For potentially cannibalistic animals such as spiders, the ability to recognize and avoid kin and/or preferentially cannibalize non-relatives would permit exploiting conspecifics as prey while minimizing loss of inclusive fitness. We investigated the effects of relatedness and availability of alternative food on cannibalism tendency in pairs of juvenile Hogna helluo (Walckenaer), a North American wolf spider (Araneae: Lycosidae). For second-instar spiderlings (dispersing stage), cannibalism was more likely among pairs of non-sibs than pairs of sibs and, interestingly, was also more likely when other prey were available. We found no evidence of increased cannibalism in pairings involving broods of greatest average size disparity, indicating that size differences are unlikely to explain differences in cannibalism tendency. Additionally, the relative number of deaths from cannibalism or other causes did not increase with increasing risk of starvation. For third-instar spiderlings, which had lived independently of their mother and sibs following dispersal, cannibalism rates were very high in all treatments and there were no significant effects of relatedness or food availability. Our results suggest that spiders with predominantly solitary lifestyles may bias cannibalism toward non-kin during the juvenile associative period, and that this effect is lost in the subsequent instar. Results are discussed in the context of several potential mechanisms that might result in differential cannibalism.Communicated by M. Elgar     

Paternal kin bias in the agonistic interventions of adult female rhesus macaques (Macaca mulatta)

When agonistic interventions are nepotistic, individuals are expected to side more often with kin but less often against kin in comparison with non-kin. As yet, however, few mammal studies have been in a position to test the validity of this assertion with respect to paternal relatedness. We therefore used molecular genetic kinship testing to assess whether adult female rhesus macaques (Macaca mulatta) from the free-ranging colony of Cayo Santiago (Puerto Rico) bias their interventions in ongoing dyadic aggressive interactions towards maternal and paternal half-sisters compared with unrelated females. It turned out that females supported maternal half-sisters significantly more often than paternal half-sisters or non-kin regardless of the costs associated with such interventions. Similarly, females targeted maternal half-sisters significantly less often than non-kin when this was associated with high costs. Unrelated females provided significantly higher mean rates of both high- and low-cost support to each other than did paternal half-sisters. However, females targeted paternal half-sisters significantly less often than non-kin when targeting was at low cost, suggesting that females refrain from intervening against paternal half-sisters. Our data confirm the general view that coalition formation in female mammals is a function of both the level of maternal relatedness and of the costs of intervention. The patterns of coalition formation among paternal kin were found to be more complex, and may also differ across species, but clear evidence for paternal kin discrimination was observed in female rhesus as predicted by kin selection theory.     

Benefits of kin association: related and familiar zebrafish larvae (<Emphasis Type="Italic">Danio rerio</Emphasis>) show improved growth

Zebrafish (Danio rerio) larvae prefer the olfactory cues of kin to non-kin. We examined the potential benefits of kin preference by comparing growth rate, shoaling, and aggressive behavior in juvenile zebrafish housed in groups of either familiar kin or unfamiliar non-kin. Over an observation period of 5 days, the animals grew 33% more in kin groups; however, neither shoaling nor the frequency of aggressive interactions was different in groups of related versus unrelated individuals. Shoaling behavior increased with increasing observation time and increasing age, while aggressive behavior remained the same. We conclude that associating with kin probably creates a less stressful environment that allows for higher growth rates, which can lead to higher direct fitness based on increased survival and earlier reproduction. Kin recognition leading to kin-structured groups may therefore be under positive selection.     

Factors influencing sexual cannibalism and its benefit to fecundity and offspring survival in the wolf spider Pardosa pseudoannulata (Araneae: Lycosidae)

Sexual cannibalism is hypothesized to have evolved as a way to obtain a high-quality meal, as an extreme mate choice or as a consequence of female aggressive spillover. Here, we examined underlying factors likely to influence sexual cannibalism in the wolf spider Pardosa pseudoannulata (Bösenberg & Strand, 1906) from China, including mating status, female egg-laid status, female hunger level, female adult age and mate size dimorphism. The results showed that about 10 % of P. pseudoannulata virgin females cannibalized the approaching males before mating and that 28 % of P. pseudoannulata virgin females immediately cannibalized the males after mating. No incidents of sexual cannibalism during copulation were observed. Before mating, previously mated females and starved females tended to engage in significantly higher rates of attacks compared to virgin and well-fed females. Females that had laid egg sacs tended to engage in a significantly higher rate of attacks and sexual cannibalism than virgin females before mating. Regardless of pre- or post-mating, there was a strong positive relationship between mate size dimorphism and the occurrence of sexual cannibalism. We also tested the effects of sexual cannibalism on the fecundity of cannibalistic females and the survival of their offspring. Our results indicated that sexual cannibalism affected positively the offspring survival of cannibalistic females, but not fecundity. Our findings support the hypothesis that sexual cannibalism has evolved as an adaptive component of female foraging strategy and that it benefits offspring survival as a result of paternal investment.     

Differential aggressiveness between fire salamander (<Emphasis Type="Italic">Salamandra infraimmaculata</Emphasis>) larvae covaries with their genetic similarity

Responding differentially to kin and non-kin is known to be adaptive in many species. One example is the inclusive fitness benefits of reducing aggression toward closer relatives. Little is known, however, about the ability of animals to assess differential degrees of genetic relatedness and to respond accordingly with differential levels of aggression. In the present study, we tested whether aggressiveness between body mass-matched pairs of fire salamander (Salamandra infraimmaculata) larvae covaried with the genetic similarity between them. We quantified aggressiveness at three levels of genetic similarity by selecting pairs within and across pools from recently genotyped populations. We also assessed aggression between pairs of siblings. Aggression and associated injuries decreased as genetic similarity increased across the groups. These findings suggest that cannibalistic salamanders can assess their degree of genetic relatedness to conspecifics and vary their behavioral responses depending on the degree of similarity between them along a genetic relatedness continuum.     

Changes in metabolic substrates during early development in anchoveta Engraulis ringens (Jenyns 1842) in the Humboldt Current

We assessed the ontogenetic changes in protein content and free amino acids (FAA) in eggs and early larvae of Engraulis ringens (anchoveta) off central Chile on different dates during the spawning season. On all sampling dates, a reduction in embryonic yolk-sac volume, proteins and FAA concentrations occurred during development. Protein electrophoresis (SDS–PAGE) of eggs and larvae showed at least 22 protein bands: 11 were consumed early and not detected after hatching. The proportion of essential FAA (EFAA) was higher than the proportion of non-essential FAA (NEFAA) in early eggs and in 7 day-old larvae (82.5-73% EFAA respectively). During egg development, the FAA pool was dominated by leucine, alanine and lysine, three amino acids contributing 35–44% of the total FAA in eggs. During larval development, histidine was the most abundant FAA. In July, total FAA constituted 13–18% of the egg dry weight. A similar proportion (45–51%) occurred in July between protein plus FAA and total lipids. The differences in egg size during the spawning season along with variability in batch composition suggests that the female spawning condition is a major factor determining egg quality and early offspring success.     

Kin and population recognition in sympatric Lake Constance perch (Perca fluviatilis L.): can assortative shoaling drive population divergence?

Prior studies have shown that perch (Perca fluviatilis L.) of Lake Constance belong to two genetically different but sympatric populations and that local aggregations of juveniles and adults contain closely related kin. In this study, we analysed the genetic structure of pelagic perch larvae to investigate if kin-structured shoals already exist during early ontogenetic development or might be the result of homing to natal sites. Analysis of the gene frequencies at five microsatellite loci revealed that three out of five pelagic aggregations of larvae showed significant accumulation of kin. To investigate possible mechanisms of shoal formation, we tested if perch use olfactory cues to recognize their kin. Choice tests in a fluviarium showed preference for odours of unfamiliar kin vs unfamiliar non-kin. Additionally, we showed that perch could differentiate between the odours of the two sympatric populations and significantly preferred unfamiliar and unrelated conspecifics of their own over the foreign population. Our results present a behavioural mechanism that can lead to the observed formation of kin-structured shoals in perch. We further discuss if the ability to discriminate between their own and a foreign population can result in assortative mating within populations and thus form the basis of “socially mediated speciation” in perch.     

Ladybird mothers mitigate offspring starvation risk by laying trophic eggs

A large proportion of ladybird beetle (Coleoptera: Coccinellidae) eggs are apparently infertile—they do not develop an embryo and are consumed by larvae hatching within the egg batch. The predicted benefits of egg consumption for larvae are empirically well supported. An important question, however, remains: are these eggs a maternal strategy to feed offspring (i.e., trophic eggs) or did egg eating evolve to exploit unavoidably infertile eggs? We investigated the adaptive value of infertile eggs in laboratory experiments with multicoloured Asian ladybirds (Harmonia axyridis). Female H. axyridis were assigned to low and high resource environments for brief intervals; we predicted that tactics to facilitate egg cannibalism, such as infertile egg production and hatching asynchrony, would be adopted in low food environments in which starvation risk for offspring is greater. We conducted two experiments in this manner that provided females with information about resource levels through prey feeding or scent. We also observed female oviposition patterns and tested for infertile egg distributions that departed from random. Females produced 56% more infertile eggs in the low vs. the high food treatment; however, hatching synchrony did not change. We consider a potential confound between information and nutrition state unlikely because ladybirds are well able to tolerate low food for 24 h, the duration of trials, and because females were in good condition when trials began. Results suggest that ladybirds use information from prey encounter to manipulate the proportion of trophic eggs in a manner consistent with the adaptive hypothesis, the first evidence of trophic egg plasticity in a non-eusocial insect.     

Oviposition height increases parasitism success by the robber fly Mallophora ruficauda (Diptera: Asilidae)

For parasitoids, host finding is a central problem that has been solved through a variety of behavioural mechanisms. Among species in which females do not make direct contact with hosts, as is the case for many dipteran parasitoids, eggs must be laid in an appropriate part of the host habitat. The asilid fly Mallophora ruficauda lays eggs in clusters on tall vegetation. Upon eclosion, pollen-sized larvae fall and parasitize soil-dwelling scarab beetle larvae. We hypothesized that wind dissemination of M. ruficauda larvae is important in the host-finding process and that females lay eggs at heights that maximize parasitism of its concealed host. Through numerical and analytical models resembling those used to describe seed and pollen wind dispersal, we estimated an optimal oviposition height in the 1.25- to 1.50-m range above the ground. Our models take into account host distribution, plant availability and the range over which parasitic larvae search for hosts. Supporting our findings, we found that the results of the models match heights at which egg clusters of M. ruficauda are found in the field. Generally, work on facilitation of host finding using plants focuses on plants as indicators of host presence. We present a case where plants are used in a different way, as a means of offspring dispersal. For parasitoids that carry out host searching at immature stages rather than as adults, plants are part of a dissemination mechanism of larvae that, as with minute seeds, uses wind and a set of simple rules of physics to increase offspring success.     

Paternity and condition affect cannibalistic behavior in nest-tending bluegill sunfish

Theory of parental care evolution predicts that a parent should invest more in a brood when its fitness value is greater than alternative investments such as the parent's own survivorship or future broods. In fish, filial cannibalism (eating one's own offspring) is widespread and represents a challenge to parental care evolution. In this study, I investigated filial cannibalism in bluegill sunfish (Lepomis macrochirus). Bluegill are characterized by alternative mating tactics referred to as "parentals" and "cuckolders". Parentals delay maturation, construct nests, court females and provide sole parental care for the developing offspring. Cuckolders mature precociously and parasitize parentals using two tactics called "sneakers" and "satellites". I found that parentals that obtained fewer eggs during spawning appeared more likely to completely cannibalize their brood (total filial cannibalism: P=0.07), regardless of their condition. Among parentals that provided care, partial cannibalism was greater during the egg phase as compared to the fry phase of care, but it was unrelated to brood size. Throughout the care period, parentals in better condition were less likely to partially cannibalize their brood, indicating that parentals use cannibalism to replenish energy reserves. Independent of condition, parentals that were cuckolded more were more likely to eat part of their brood. This relationship was evident only after the eggs had hatched, which is consistent with data showing that parentals can use olfactory cues produced by fry but not eggs to assess their paternity. This latter result proposes that parentals may be selectively culling cuckolder offspring from their nest. These data provide empirical support for parental care theory, and the first evidence for the importance of paternity on cannibalistic behavior.Communicated by M. Abrahams     

Nestmate recognition for eggs in the honeybee (<Emphasis Type="Italic">Apis mellifera</Emphasis> L.)

Colony integrity is fundamental to social insects and is threatened by the reproduction of non-nestmates. Therefore, discrimination between eggs derived from nestmates and non-nestmates would constitute an adaptation to prevent exploitation of the entire cooperative group by unrelated individuals. The removal of nestmate and non-nestmate queen and worker-laid eggs was evaluated in honeybees using colonies of Apis mellifera capensis to test female and of A. m. scutellata to test male eggs. The data show that honeybees can distinguish between nestmate and non-nestmate eggs of both sexes. Moreover, non-nestmate female queen-laid eggs were removed significantly faster than nestmate female worker-laid eggs in A. m. capensis, indicating that nestmate recognition cues can override caste-specific ones. While the experimental manipulation accounts for 37.2% (A. m. scutellata) or 1.6% (A. m. capensis) of variance in relation to egg removal, nestmate recognition explains 33.3% for male eggs (A. m. scutellata) and 60.6% for female eggs (A. m. capensis), which is almost twice as high as the impact of caste (16.7% A. m. scutellata; 25% A. m. capensis). Our data show a stronger effect of nestmate recognition on egg removal in the honeybee, suggesting that cues other than caste-specific ones (viability/kin) can dominate egg removal behavior. In light of intraspecific social parasitism, preventing the reproduction of unrelated individuals (group selection) rather than preferring queens’ eggs (kin selection) appears to be the driving force behind the evolution of egg removal behavior in honeybees.     

Old but gold: males preferentially cannibalize young eggs

Although counterintuitive at first sight, filial cannibalism is common in the animal kingdom and has been recognized as a mechanism to increase the cannibalizing parent’s lifetime reproductive success. However, previous evidence is often inconclusive and the adaptiveness of filial cannibalism is still not fully understood. We here address the notion that parents do not cannibalize at random but preferably consume offspring with a particular phenotype. To assess if differences in developmental stage and thus reproductive value of eggs trigger such selectivity, we experimentally presented male common gobies (Pomatoschistus microps) with two differently aged egg clutches within mixed broods. We found that males consumed significantly more young than old eggs. This result indicates that parents are not only able to discriminate between eggs based on developmental stage, but might use this to reduce the cost of partial filial cannibalism by selectively removing eggs of lower reproductive value.     

Sex,cannibalism and sticklebacks

Summary Two closely related species of sticklebacks (Pisces:Gasterosteidae), breeding in the same site at the same time, showed different patterns of egg cannibalism. In Gasterosteus aculeatus the intensity of cannibalism was density-dependent and females were the most important cannibals. In G. wheatlandi cannibalism was not density-dependent and males ate more eggs than females. This study indicates that sex-specific patterns of cannibalism can differ widely between species despite their similar ecology, and it provides evidence inconsistent with a currently popular explanation for egg cannibalism.     

Worker policing and nest mate recognition in the ant <Emphasis Type="Italic">Formica fusca</Emphasis>

A conflict over male production arises in social insects where workers are able to lay unfertilized male eggs. This happens because each female (queen or worker) is most closely related to her own sons and is thus predicted to reproduce. The conflict is modulated by worker policing where workers prevent each other from reproducing by aggression or egg cannibalism. In this study, we show that in the ant Formica fusca, worker policing occurs by egg cannibalism rather than by overt aggression among workers. Furthermore, we show that, contrary to bees, wasps and other ant species, egg discrimination in F. fusca is not based only on a universal queen signature chemical and that nest mate recognition of eggs occurs.     

Genetic relatedness and eusociality: parasite-mediated selection on the genetic composition of groups

Summary Contrary to the expectations of kin selection theory, intracolony relatedness in eusocial insects is often low. We examined the idea that associations of low relatedness (high genetic variability) may be advantageous because of negative frequency-dependent selection on common host phenotypes by rapidly evolving parasites and pathogens. Using the natural host-parasite system of the bumble bee Bombus terrestris and its intestinal trypanosome Crithidia bombi, we investigated the transmission properties of parasites in host groups. Within naturally infested nests and in artificially constructed groups of workers, prevalence of infestation increased with time of exposure (Table 1). The susceptibility of isolated groups of workers to the parasites to which they were exposed differed with identity and natural infestation of their nest of origin (Table 2). In addition, those workers that were related to the individual introducing an infection to their group were more likely to become infested than were unrelated workers (Table 3). Although the bumble bee workers in experimental boxes appeared to differ in behavior toward kin and non-kin, making more physical contacts with kin, we found no discernible relationship between number of physical contacts and prevalence of infestation in a group. Therefore, we conclude that differences in parasite transmission reflected interactions among different host and parasite phenotypes. This system thus demonstrates the factors necessary for negative frequency-dependent selection by parasites on common host phenotypes - variability for susceptibility and infectiousness in host and parasite populations and similarity for these traits among related individuals. If, as we show here, high genetic relatedness within groups enhances parasite transmission, kin directed altruism may increase the risk of contracting parasites and infectious diseases. Therefore, parasites and pathogens may be an important force moderating the genetic structure of social groups. Offprint requests to: J.A. Shykoff at the present address     

Hydrography and distribution dynamics of larval and juvenile fishes in the coastal waters of the Tanshui River estuary,Taiwan, with reference to estuarine larval transport

Distribution dynamics of fish larvae and juveniles in the coastal waters of the Tanshui River, Taiwan was studied fortnightly using surface horizontal tows with a larval net in daytime during the period from early April through early June 1991. Environmental factors, including water temperature, salinity, dissolved oxygen, pH, transparency and depth at sampling stations, were also monitored. A total of 10737 fish eggs and 1387 individuals, representing 43 families and 93 species, was collected during five cruises from 12 stations in the coastal waters. Most fish were estuarine-dependent marine species. Liza macrolepis, Ambassis gymnocephalus, Terapon jarbua, Mullidae and Gobiidae were the most dominant, making up 64.7% of the total catch. Early life stages, including egg, preflexion, flexion and postflexion larvae were abundant in surface samples. However, yolk-sac larvae were absent in the surface water, probably due to an ontogenetic behavioral shift as a consequence of a change in specific weight during early development. The species composition of fish larvae and juveniles was related to the microhabitats found in the coastal waters. The physico-chemical conditions, along with ontogenetic behavior, played an important role in larval fish distribution in the coastal waters.     

Female sand gobies gain direct benefits by choosing males with eggs in their nests

In some fish species with paternal care, females prefer to spawn with males whose nests already contain eggs. Several hypotheses have been put forward to explain this behaviour, such as reduced risk of predation or cannibalism (the dilution effect), increased parental investment, and mate copying. This experimental study focuses on female mate choice in the sand goby, Pomatoschistus minutus. Females were found to choose males with eggs in their nests. In addition, hatching success increased with clutch size, mainly because males with larger clutches showed less filial cannibalism. Increased egg survival in large clutches may thus be explained by a combination of the dilution effect and higher parental investment. In another experiment, females did not seem to copy the observed mate choice of other females. In conclusion, female preference for males with eggs in their nests is adaptive, and can be explained by direct benefits, as more surviving offspring are produced. Received: 23 December 1995/Accepted after revision: 11 May 1996     

Kin and non-kin interventions in the aggressive disputes of vervet monkeys

Summary Interventions in aggressive disputes were investigated in a free-living troop of vervets (Cercopithecus aethiops sabaeus) in Barbados. Interventions on behalf of kin were more frequent than on behalf of non-kin. Both types of interventions were more likely when the intervening animal outranked the opponent; presumably because retaliation probability, and hence cost of intervening, is low against low ranking opponents. The number of interventions given on behalf of both kin and non-kin increased with the number of disputes in which they were involved. In contrast to kin interventions, the number of interventions given on behalf of non-kin was correlated with that received by non-kin, suggesting that reciprocation is a necessary component of non-kin interventions. Non-kin interventions were more likely when the recipient outranked the opponent, presumably because reciprocation probability is high. Pairs of non-kin form structured reciprocal relationships based on the proportion of interventions allocated to each other, and most non-kin interventions flowed through these relationships. Males intervened on behalf of non-kin more frequently than did females. The implications of the results for the evolution of kin and reciprocal altruism were discussed.