Kin Recognition Research Articles

Major evolutionary transitions in individuality

The evolution of life on earth has been driven by a small number of major evolutionary transitions. These transitions have been characterized by individuals that could previously replicate independently, cooperating to form a new, more complex life form. For example, archaea and eubacteria formed eukaryotic cells, and cells formed multicellular organisms. However, not all cooperative groups are en route to major transitions. How can we explain why major evolutionary transitions have or haven’t taken place on different branches of the tree of life? We break down major transitions into two steps: the formation of a cooperative group and the transformation of that group into an integrated entity. We show how these steps require cooperation, division of labor, communication, mutual dependence, and negligible within-group conflict. We find that certain ecological conditions and the ways in which groups form have played recurrent roles in driving multiple transitions. In contrast, we find that other factors have played relatively minor roles at many key points, such as within-group kin discrimination and mechanisms to actively repress competition. More generally, by identifying the small number of factors that have driven major transitions, we provide a simpler and more unified description of how life on earth has evolved.

Maternal Transfer of Cuticular Hydrocarbons? Evidence from Between-Species Cross-Fostering Experiments in Earwigs

When females care for broods of mixed paternity, there is a threat of enhanced rivalry among offspring of different paternal lineages. This competition is against the best evolutionary interest of the female because she is equally related to all of her offspring and enhanced offspring competition would decrease her fitness. It was hypothesized earlier that mothers should therefore conceal the information about paternal origin in the recognition cues used by her offspring, for example by transferring the chemical cues used by her offspring for kin recognition. Here, we used a cross-fostering experiment between two closely related and sympatric earwig species, Forficula auricularia and F. decipiens, to demonstrate that F. auricularia nymphs tended by F. decipiens females differ in their cuticular hydrocarbon profiles from F. auricularia nymphs tended by F. auricularia females. This result provides evidence for maternal transfer of cuticular hydrocarbons and shows that offspring adoption across species is possible in earwigs.

Male rank, not paternity, predicts male–immature relationships in mountain gorillas, Gorilla beringei beringei

Kin discrimination mechanisms are expected to evolve when they provide fitness benefits. To date, evidence for kin discrimination is mixed across taxa and mating systems even when it would apparently be beneficial. In animals with promiscuous mating systems, males were long believed to abstain from parenting behaviours partly because the costs of offspring misidentification outweighed the benefits of dual parenting. Conversely, males in monogamous systems could parent because of high paternity certainty. However, recent work has shown that in some species males parent despite high false paternity rates, and males in some promiscuous systems discriminate between their own and other males' offspring. Here we evaluate the impact of male dominance rank, paternity and age on maleeimmature relationships in wild mountain gorillas. Mountain gorillas provide an interesting context for assessing paternal kin discrimination because (1) maleeimmature relationships are strong, and (2) while their morphological characteristics suggest an evolutionary history of single-male groups, a substantial fraction contain multiple adult males. In our sample of 21 males and 49 genotyped immatures living in multimale groups monitored by the Dian Fossey Gorilla Fund's Karisoke Research Center, we found that male rank was the primary predictor of maleeimmature relationship strength. There was little evidence that paternity or age were related to relationship patterns. Maleeimmature dyads were closer social partners in 2011e12 when groups were smaller and reproductive skew lower, than comparable dyads in 2003e04 when groups were larger and skew higher. Gorillas' lack of paternal kin discrimination provides further behavioural evidence that the species' multimale social structure is evolutionarily novel. However, patterning of maleeimmature relationships and genetic paternity suggest a persistent minority of two-male groups throughout G. beringei's evolutionary history. This may help explain their ability to live in multimale, multifemale social units despite possessing morphological characteristics typical of harem systems.

Mechanisms of inbreeding avoidance in the one-piece drywood termite Neotermes chilensis

Inbreeding depression refers to a decrease in fitness components in the offspring of closely related sexual pairs. Given the disadvantages of inbreeding depression, it is of interest to study the mechanisms involved in its avoidance, particularly in social insects. In termites, colonies are founded by dispersing individuals. Two types of mechanisms may account for inbreeding avoidance: indirect mechanisms that occur before the dispersing individuals come into contact (sex-biased production at colony level, sex-biased emergence timing, dispersal, and sex-biased dispersal), and an active mechanism (kin recognition) that occurs when dispersing individuals come into contact. We have used ecological, behavioral and genetic approaches to study the mechanisms of inbreeding avoidance along the complete process of colony foundation by Neotermes chilensis, i.e., from the production of dispersing individuals in the colony to the production of siblings by the newly formed reproductive pair. This is the first report to address both indirect and active mechanisms of inbreeding avoidance in the same study, in the same termite species, and through the complete process of colony foundation. The results show that dispersal is the main indirect mechanism of inbreeding avoidance and that kin recognition is unlikely as an active mechanism of inbreeding avoidance.

Clonal composition of colonies of a eusocial aphid, Ceratovacuna japonica

High degrees of relatedness among colony mates and kin recognition ability are important factors maintaining eusociality. However, in eusocial aphids, clone mixing between different colonies is reported to occur frequently, suggesting a lack of kin recognition. Studies investigating the clonal composition of eusocial aphid colonies have focused on the aphid generation on the primary host plant (gall generation). To test whether clone mixing also occurs in open colonies of eusocial aphids on their secondary host plants (open-colony generation), we carried out an amplified fragment length polymorphism analysis to investigate clonal composition within colonies of the eusocial aphid Ceratovacuna japonica . The results showed that clone mixing occurred frequently in open-colony generation.

The use of acoustic playbacks with captive cetaceans

Playbacks are a powerful tool in studies of animal communication and cognition. They can provide insights into referentiality, social memory, anti-predator strategies, sexual selection, as well as a host of other topics. In particular, playbacks have been a useful method for understanding the nature of wild dolphin communication using temporarily restrained animals. Unfortunately, there are a series of questions where complete social histories of subjects or certain controls are needed, but unavailable in wild study populations. Captive, free-swimming animals present a complementary set of subjects where one can address questions involving referentiality or dolphin social memory. Methods for conducting playbacks with captive groups differ greatly than for wild subjects. I will explore the procedural differences of these experiments, including overcoming difficulties associated with recording and presenting sounds in an acoustically challenging environment as well as how to measure response behavior. Furthermore, I will discuss the potential of captive acoustic playbacks by highlighting data collected from such studies including evidence for dolphin multi-decade social memory, context dependent cue usage and acoustic kin recognition.

Human kin detection.

Natural selection has favored the evolution of behaviors that benefit not only one's genes, but also their copies in genetically related individuals. These behaviors include optimal outbreeding (choosing a mate that is neither too closely related, nor too distant), nepotism (helping kin), and spite (hurting non-kin at a personal cost), and all require some form of kin detection or kin recognition. Yet, kinship cannot be assessed directly; human kin detection relies on heuristic cues that take into account individuals' context (whether they were reared by our mother, or grew up in our home, or were given birth by our spouse), appearance (whether they smell or look like us), and ability to arouse certain feelings (whether we feel emotionally close to them). The uncertainties of kin detection, along with its dependence on social information, create ample opportunities for the evolution of deception and self-deception. For example, babies carry no unequivocal stamp of their biological father, but across cultures they are passionately claimed to resemble their mother's spouse; to the same effect, 'neutral' observers are greatly influenced by belief in relatedness when judging resemblance between strangers. Still, paternity uncertainty profoundly shapes human relationships, reducing not only the investment contributed by paternal versus maternal kin, but also prosocial behavior between individuals who are related through one or more males rather than females alone. Because of its relevance to racial discrimination and political preferences, the evolutionary pressure to prefer kin to non-kin has a manifold influence on society at large.

Demographic mechanisms of inbreeding adjustment through extra-pair reproduction.

One hypothesis explaining extra-pair reproduction is that socially monogamous females mate with extra-pair males to adjust the coefficient of inbreeding (f) of extra-pair offspring (EPO) relative to that of within-pair offspring (WPO) they would produce with their socially paired male. Such adjustment of offspring f requires non-random extra-pair reproduction with respect to relatedness, which is in turn often assumed to require some mechanism of explicit pre-copulatory or post-copulatory kin discrimination. We propose three demographic processes that could potentially cause mean f to differ between individual females’ EPO and WPO given random extra-pair reproduction with available males without necessarily requiring explicit kin discrimination. Specifically, such a difference could arise if social pairings formed non-randomly with respect to relatedness or persisted non-randomly with respect to relatedness, or if the distribution of relatedness between females and their sets of potential mates changed during the period through which social pairings persisted. We used comprehensive pedigree and pairing data from free-living song sparrows (Melospiza melodia) to quantify these three processes and hence investigate how individual females could adjust mean offspring f through instantaneously random extra-pair reproduction. Female song sparrows tended to form social pairings with unrelated or distantly related males slightly less frequently than expected given random pairing within the defined set of available males. Furthermore, social pairings between more closely related mates tended to be more likely to persist across years than social pairings between less closely related mates. However, these effects were small and the mean relatedness between females and their sets of potential extra-pair males did not change substantially across the years through which social pairings persisted. Our framework and analyses illustrate how demographic and social structuring within populations might allow females to adjust mean f of offspring through random extra-pair reproduction without necessarily requiring explicit kin discrimination, implying that adjustment of offspring f might be an inevitable consequence of extra-pair reproduction. New theoretical and empirical studies are required to explore the general magnitude of such effects and quantify the degree to which they could facilitate or constrain long-term evolution of extra-pair reproduction.

Perspectives: Hamilton's Legacy: Mechanisms of Kin Recognition in Humans

The behavior literature is replete with examples of individuals exhibiting costly acts that benefit someone else. These examples troubled Darwin so much so that he thought they would be fatal to his theory of natural selection. A century later, W. D. Hamilton refined that theory by showing, quantitatively, that such acts could be favored if the individuals involved were relatives. His theory of inclusive fitness is generally considered one of the greatest theoretical advances in evolution since Darwin's time. Less appreciated from Hamilton's 1964 paper is the hypothesis that mechanisms favoring accurate kin recognition will also be selected. Here, I review those recognition mechanisms and survey the literature on human kin recognition. Although not often considered, humans both produce cues to kinship that vary with genetic relatedness and have perceptual abilities to detect these cues in others and assess that relatedness. The potential functions of these abilities are discussed. Importantly, gaps in our understanding of the development and use of recognition mechanisms are noted.

Kin recognition in Setaria italica under the condition of root segregation

Kin recognition in Setaria italica under the condition of root segregation

Female sociality and kin discrimination in brood parasitism: unrelated females fight over egg laying

In conspecific brood parasitism, some females (“parasites”) lay eggs in nests of other females of the same species (“hosts”). This reproductive tactic is particularly common in waterfowl, in which studies suggest that parasites are often related to the host. Here, we test the hypothesis that hosts may discriminate and reject unrelated parasites. Based on observations and >4100h of digital video film, we analyze behavioral interactions at 65 nests of High Arctic common eiders during the laying sequence. We also estimate parasitism and host–parasite relatedness by albumen fingerprinting of 975 eggs from 232 nests. Among the video-filmed nests in which interactions were recorded during the egg-laying period, 11 had eggs from 2 females. At 8 of these 11 nests, there was overt female aggression and significantly lower host–parasite relatedness (mean coefficient of relationship r = −0.40) than in the nests with tolerant or no interactions (r = 0.91). The results demonstrate active female kin discrimination in common eiders, used against nonrelatives that try to lay eggs in the nest. Other females trying to access the nest were often prevented from doing so: in 65% of 34 such attempts, the sitting female rejected the intruder. Brood “parasitism” in eiders and other waterfowl is complex, ranging from violent female conflict and parasitic exploitation of the host’s parental care to nest takeover and potential kin selection favoring acceptance of related parasites. These and other aspects of female sociality in eiders are discussed; in some respects, they may resemble certain long-lived matriarchal mammals.

Recent advance of kin recognition in plant

Recent advance of kin recognition in plant

Kin discrimination in tadpoles of Hylarana temporalis (Anura: Ranidae) and Sphaerotheca breviceps (Anura: Dicroglossidae) hydroperiod and social habits

A habilidade de discriminação de parentesco foi estudada em girinos de Hylarana temporalis e Sphaerotheca breviceps, que vivem em dois diferentes habitats; a primeira espécie apresenta agregação social e a segunda vive dispersa. No início do desenvolvimento, os girinos de H. temporalis são encontrados em pequenas agregações nos riachos dos Ghats Ocidentais, mas em estágios avançados são geralmente vistos em poças isoladas associadas ao leito principal após a seca do riacho. Sphaerotheca breviceps reproduz-se durante as monções de sudoeste em lagoas formadas pelas chuvas, e seus girinos são sempre encontrados dispersos. Trabalhamos com a hipótese de que os girinos que vivem agregados exibem discriminação de parentesco, enquanto aqueles que não formam agregações podem não exibir essa discriminação. Além disso, os girinos que enfrentam ameaça de dessecamento podem também não exibir comportamento de discriminação de parentesco. Foram conduzidos testes com girinos das duas espécies acima em dois estágios de desenvolvimento (Gosner 28-30 e 34-36) para descobrir sua escolha de associação com irmãos ou não-irmãos. Os girinos de H. temporalis associaram-se tanto com irmãos familiares (criados com irmãos) como irmãos não-familiares (criados em isolamento) nos estágios iniciais do desenvolvimento, mas não nos estágios finais. Os girinos de S. breviceps não mostraram preferência de associação com irmãos (familiares ou não) tanto nos estágios iniciais como nos finais. As descobertas relacionadas a H. temporalis sugerem que a discriminação de parentesco entre irmãos e não-irmãos pode ser benéfica durante os estágios iniciais do desenvolvimento que ocorre em riachos, e pode ser menos importante nos estágios finais do desenvolvimento em corpos d’água sujeitos ao dessecamento. A ausência do reconhecimento de parentesco em S. breviceps está associada à ausência de agregação natural e à ameaça de dessecamento de lagoas temporárias. Sugerimos que o comportamento de discriminação de parentesco em girinos está relacionado aos seus hábitos sociais e ao hidroperíodo de seu habitat.

The role of density and relatedness in wild juvenile A tlantic salmon growth

Growth is a key life-history trait in fish that is influenced by both abiotic (such as temperature and water chemistry) and biotic factors (such as density and food availability). Investigating how growth performance is influenced by such factors in the wild is important for understanding how population processes influence animals in natural environments and for predicting the response to conservation and management strategies that manipulate these conditions. The theory of kin selection predicts that significant growth and survival benefits are conferred upon animals associating with close relatives. However, resource competition may be more intense among close relatives, and little is known about the trade-off between these two processes under different ecological conditions. Here, we examine the correlation between naturally occurring densities and kin-biased growth rate using a species where kin recognition has a strong impact on behaviour in laboratory studies, but where, paradoxically, field investigations have failed to document predicted kin-biased growth or survival. Intra- and inter-family differences in growth rate of juvenile Atlantic salmon Salmo salar were studied to examine how relatedness (groups of full-sibling fish and groups of mixed-sibling fish) and sibling group (family/genotype) affect salmon parr growth, and the correlation of growth rate under a range of naturally occurring densities. Parentage and relatedness of neighbouring fish were assigned using microsatellite and passive integrated transponder tags, which allowed the growth estimation of individual fish. The results show that growth rate was significantly influenced by both sibling group (family of origin) and also by an interaction between relatedness and density. The latter finding indicates that at higher densities, full-sibling groups achieved higher growth rates in comparison to mixed-sibling groups. Thus, the growth benefits of associating with relatives are not conferred under all ecological conditions, but it becomes most apparent at high density when resource competition is greatest.

Shedding light on kin recognition response in plants.

Shedding light on kin recognition response in plants.

Consequences of genetic incompatibility on fitness and mate choice: the male point of view

Hymenopterans under single-locus complementary sex determination (sl-CSD) face inbreeding costs due to this sex determination mode. Under sl-CSD, homozygote eggs at the sl-CSD locus usually develop into unviable or sterile diploid males. Production of such costly males increases when sib-mating happens because related individuals share half of their genome. In the hymenopteran Venturia canescens (a solitary parasitoid wasp), diploid males are sterile, leading to fitness costs through genetic incompatibility between parents. Whereas the costs of producing diploid males and behavioural strategies that would reduce such costs have been studied in females, the potential fitness costs faced by males have not. Here, we aimed to investigate fitness costs that males endure after a single sib-mating and tested whether they have the ability to avoid sib-mating through kin recognition. Our results show that males have a reduced fitness (i.e. they produce fewer daughters) when mating with their sibs. We also show that males have the ability to distinguish between non-sib and sib females (i.e. kin). They use chemical marks emitted by the females to discriminate kin from non-kin. We discuss the evolution of kin recognition in males in the context of mate choice for genetic compatibility. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114, 279–286.

Reduced plant competition among kin can be explained by Jensen's inequality.

Plants often compete with closely related individuals due to limited dispersal, leading to two commonly invoked predictions on competitive outcomes. Kin selection, from evolutionary theory, predicts that competition between relatives will likely be weaker. The niche partitioning hypothesis, from ecological theory, predicts that competition between close relatives will likely be stronger. We tested for evidence consistent with either of these predictions by growing an annual legume in kin and nonkin groups in the greenhouse. We grew plant groups in treatments of symbiotic nitrogen fixing bacteria differing in strain identity and composition to determine if differences in the microbial environment can facilitate or obscure plant competition patterns consistent with kin selection or niche partitioning. Nonkin groups had lower fitness than expected, based on fitness estimates of the same genotypes grown among kin. Higher fitness among kin groups was observed in mixtures of N-fixing bacteria strains compared to single inoculations of bacteria strains present in the soil, which increased fitness differences between kin and nonkin groups. Lower fitness in nonkin groups was likely caused by increased competitive asymmetry in nonkin groups due to genetic differences in plant size combined with saturating relationships with plant size and fitness- i.e. Jensen's inequality. Our study suggests that microbial soil symbionts alter competitive dynamics among kin and nonkin. Our study also suggests that kin groups can have higher fitness, as predicted by kin selection theory, through a commonly heritable trait (plant size), without requiring kin recognition mechanisms.

Paternal signature in kin recognition cues of a social insect: concealed in juveniles, revealed in adults.

Kin recognition is a key mechanism to direct social behaviours towards related individuals or avoid inbreeding depression. In insects, recognition is generally mediated by cuticular hydrocarbon (CHC) compounds, which are partly inherited from parents. However, in social insects, potential nepotistic conflicts between group members from different patrilines are predicted to select against the expression of patriline-specific signatures in CHC profiles. Whereas this key prediction in the evolution of insect signalling received empirical support in eusocial insects, it remains unclear whether it can be generalized beyond eusociality to less-derived forms of social life. Here, we addressed this issue by manipulating the number of fathers siring clutches tended by females of the European earwig, Forficula auricularia, analysing the CHC profiles of the resulting juvenile and adult offspring, and using discriminant analysis to estimate the information content of CHC with respect to the maternal and paternal origin of individuals. As predicted, if paternally inherited cues are concealed during family life, increases in mating number had no effect on information content of CHC profiles among earwig juveniles, but significantly decreased the one among adult offspring. We suggest that age-dependent expression of patriline-specific cues evolved to limit the risks of nepotism as family-living juveniles and favour sibling-mating avoidance as group-living adults. These results highlight the role of parental care and social life in the evolution of chemical communication and recognition cues.

Photoreceptor-mediated kin recognition in plants.

Although cooperative interactions among kin have been established in a variety of biological systems, their occurrence in plants remains controversial. Plants of Arabidopsis thaliana were grown in rows of either a single or multiple accessions. Plants recognized kin neighbours and horizontally reoriented leaf growth, a response not observed when plants were grown with nonkin. Plant kin recognition involved the perception of the vertical red/far-red light and blue light profiles. Disruption of the light profiles, mutations at the PHYTOCHROME B, CRYPTOCHROME 1 or 2, or PHOTOTROPIN 1 or 2 photoreceptor genes or mutations at the TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS1 gene required for auxin (growth hormone) synthesis impaired the response. The leaf-position response increases plant self-shading, decreases mutual shading between neighbours and increases fitness. Light signals from neighbours are known to shape a more competitive plant body. Here we show that photosensory receptors mediate cooperative rather than competitive interactions among kin neighbours by reducing the competition for local pools of resources.

Evidence of Taxa-, Clone-, and Kin-discrimination in Protists: Ecological and Evolutionary Implications.

Unicellular eukaryotes, or protists, are among the most ancient organisms on Earth. Protists belong to multiple taxonomic groups; they are widely distributed geographically and in all environments. Their ability to discriminate among con- and heterospecifics has been documented during the past decade. Here we discuss exemplar cases of taxa-, clone-, and possible kin-discrimination in five major lineages: Mycetozoa (Dictyostelium, Polysphondylium), Dikarya (Saccharomyces), Ciliophora (Tetrahymena), Apicomplexa (Plasmodium) and Archamoebae (Entamoeba). We summarize the proposed genetic mechanisms involved in discrimination-mediated aggregation (self versus different), including the csA, FLO and trg (formerly lag) genes, and the Proliferation Activation Factors (PAFs), which facilitate clustering in some protistan taxa. We caution about the experimental challenges intrinsic to studying recognition in protists, and highlight the opportunities for exploring the ecology and evolution of complex forms of cell-cell communication, including social behavior, in a polyphyletic, still superficially understood group of organisms. Because unicellular eukaryotes are the evolutionary precursors of multicellular life, we infer that their mechanisms of taxa-, clone-, and possible kin-discrimination gave origin to the complex diversification and sophistication of traits associated with species and kin recognition in plants, fungi, invertebrates and vertebrates.