Mechanism Of Kin Discrimination Research Articles

The Evolution of Kin Discrimination Across the Tree of Life

Kin discrimination, the differential treatment of conspecifics based on kinship, occurs across the tree of life, from animals to plants to fungi to bacteria. When kin and nonkin interact, the ability to identify kin enables individuals to increase their inclusive fitness by helping kin, harming nonkin, and avoiding inbreeding. For a given species, the strength of selection for kin discrimination mechanisms is influenced by demographic, ecological, and life-history processes that collectively determine the scope for discrimination and the payoffs from kin-biased behavior. In this review, we explore how these processes drive variation in kin discrimination across taxa, highlighting contributions of recent empirical, comparative, and theoretical work to our understanding of when, how, and why kin discrimination evolves.

Modular Lipoprotein Toxins Transferred by Outer Membrane Exchange Target Discrete Cell Entry Pathways.

ABSTRACTBacteria compete against related individuals by delivering toxins. In myxobacteria, a key delivery and kin discrimination mechanism is called outer membrane (OM) exchange (OME). Here, cells that display compatible polymorphic cell surface receptors recognize one another and bidirectionally transfer OM content. Included in the cargo is a suite of polymorphic SitA lipoprotein toxins. Consequently, OME between compatible cells that are not clonemates results in intoxication, while exchange between clonemates is harmonious because cells express a cognate repertoire of immunity proteins, which themselves are not transferred. SitA toxins belong to six nonhomologous families classified by sequence conservation within their N-terminal “escort domains” (EDs), while their C termini contain polymorphic nucleases that target the cytoplasmic compartment. To investigate how toxins delivered to the OM by OME translocate to the cytoplasm, we selected transposon mutants resistant to each family. Our screens identified eight genes that conferred resistance in a SitA family-specific manner. Most of these genes are predicted to localize to the cell envelope, and some resemble proteins that colicins exploit to gain cell entry. By constructing functional chimeric SitAs between families, we show that the ED determines the specificity of resistance. Importantly, a mutant that confers resistance to all six SitA families was discovered. This gene was named traC and plays an accessory role with traAB in OME. This work thus provides insight into the mechanism of kin discrimination in myxobacteria and provides working models for how SitA toxins exploit host proteins to gain cytoplasmic entry.

TYPE VB AND VI SECRETION SYSTEMS AS COMPETITION AGENTS OF GRAM-NEGATIVE BACTERIA

Abstract Bacterial competition, defined as a local neighbour interactions, can lead to competitors coexistence, bacterial community self-organization or as travelling waves of species dominance in ecological niches. Bacteria have developed many mechanisms to communicate and compete. Kin discrimination mechanisms in bacterial populations allow species to distinguish a friend from a foe in bacterial environment. Type Vb and VI secretion systems (TVIbSS and TVISS) play crucial role in this phenomenon. A contact-dependent growth inhibition (CDI), primarily found in Escherichia coli strains, utilities CdiB/CdiA protein of type Vb secretion system, described also as two-partner secretion (TPS) system, to inhibit growth of non-kin strains, where cell contact is required. Presence of an intracellular small immunity protein (CdiI) protects E. coli cells from autoinhibition. Other bacterial competition system, primarily found in nodulation process of Rhizobium leguminosarum bv. Trifolii strain, engages type VI secretion system. The structure of TVISS is more complicated and comprises the series of proteins with structural homology to bacteriophage tail proteins and membrane proteins which builds the core of the system (Tss proteins). Meanwhile, other proteins of the TVISS was described as associated proteins (Tag proteins). Important proteins for TVISS are haemolysin coregulated protein (Hcp) which has hexameric, tubular structure and VgrG protein (valine-glycine repeat G) which play a dual role in the process: as a chaperone protein in secretion of effector toxin or/and as a secreted toxin itself. Despite the structural differences of both secretion systems they show functional homology in competition phenomenon and govern the social life of bacterial community. 1. Introduction. 2. Contact-dependent growth inhibition. 2.1. Structure o CDI machinery. 2.2. Effectors of CDI system. 3. Type VI secretion system. 3.1. Structure of type VI secretion system. 3.2. Effectors of type VI secretion system. 4. Membership to polymorphic toxins system. 5. Role of the systems in bacterial biology. 6. Conclusions

Mechanism of Kin-Discriminatory Demarcation Line Formation between Colonies of Swarming Bacteria

Swarming bacteria use kin discrimination to preferentially associate with their clonemates for certain cooperative behaviors. Kin discrimination can manifest as an apparent demarcation line (a region lacking cells or with much lower cell density) between antagonist strains swarming toward each other. In contrast, two identical strains merge with no demarcation. Experimental studies suggest contact-dependent killing between different strains as a mechanism of kin discrimination, but it is not clear whether this killing is sufficient to explain the observed patterns. Here, we investigate the formation of demarcation line with a mathematical model. First, using data from competition experiments between kin discriminating strains of Myxococcus xanthus and Proteus mirabilis, we found the rates of killing between the strains to be highly asymmetric, i.e., one strain kills another at a much higher rate. Then, to investigate how such asymmetric interactions can lead to a stable demarcation line, we construct reaction-diffusion models for colony expansion of kin-discriminatory strains. Our results demonstrate that a stable demarcation line can form when both cell movement and cell growth cease at low nutrient levels. Further, our study suggests that, depending on the initial separation between the inoculated colonies, the demarcation line may move transiently before stabilizing. We validated these model predictions by observing dynamics of merger between two M. xanthus strains, where one strain expresses a toxin protein that kills a second strain lacking the corresponding antitoxin. Our study therefore provides a theoretical understanding of demarcation line formation between kin-discriminatory populations, and can be used for analyzing and designing future experiments.

Using playback of territorial calls to investigate mechanisms of kin discrimination in red squirrels

Kin recognition can facilitate kin selection and may have played a role in the evolution of sociality. Red squirrels (Tamiasciurus hudsonicus) defend territories using vocalizations known as rattles. They use rattles to discriminate kin, though the mechanism underlying this ability is unknown. Our objective was to distinguish between the mechanisms of prior association, where animals learn the phenotypes of kin they associate with early in life, and phenotype matching/recognition alleles, where animals use a template to match phenotypes, thereby allowing them to recognize kin without an association early in life. We used audio playbacks to measure the responses of squirrels to rattles from familiar kin, unfamiliar kin, and non-kin. Initial analyses revealed that red squirrels did not discriminate between familiar and unfamiliar kin, but also did not discriminate between kin and non-kin, despite previous evidence indicating this capability. Post hoc analyses showed that a squirrel’s propensity to rattle in response to playback depended on an interaction between relatedness and how the playback stimuli had been recorded. Red squirrels discriminated between rattles from close kin (r = 0.5) and rattles from non-kin (r < 0.125) when the rattles were recorded from provoked squirrels. Squirrels did not exhibit kin discrimination in response to unsolicited rattles. Once we accounted for how the stimuli had been recorded, we found no difference in the responses to familiar and unfamiliar kin. Our study suggests that kin discrimination by red squirrels may be context dependent.

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.

Chimaeric load among sympatric social bacteria increases with genotype richness.

The total productivity of social groups can be determined by interactions among their constituents. Chimaeric load--the reduction of group productivity caused by antagonistic within-group heterogeneity--may be common in heterogeneous microbial groups due to dysfunctional behavioural interactions between distinct individuals. However, some instances of chimaerism in social microbes can increase group productivity, thus making a general relationship between chimaerism and group-level performance non-obvious. Using genetically similar strains of the soil bacterium Myxococcus xanthus that were isolated from a single centimetre-scale patch of soil, we tested for a relationship between degree of chimaerism (genotype richness) and total group performance at social behaviours displayed by this species. Within-group genotype richness was found to correlate negatively with total group performance at most traits examined, including swarming in both predatory and prey-free environments and spore production during development. These results suggest that interactions between such neighbouring strains in the wild will tend to be mutually antagonistic. Negative correlations between group performance and average genetic distance among group constituents at three known social genes were not found, suggesting that divergence at other loci that govern social interaction phenotypes is responsible for the observed chimaeric load. The potential for chimaeric load to result from co-aggregation among even closely related neighbours may promote the maintenance and strengthening of kin discrimination mechanisms, such as colony-merger incompatibilities observed in M. xanthus. The findings reported here may thus have implications for understanding the evolution and maintenance of diversity in structured populations of soil microbes.

“Armpit effect” in an African cichlid fish: self-referent kin recognition in mating decisions of male Pelvicachromis taeniatus

Kin discrimination in nepotistic as well as in sexual contexts is widespread in animals including humans. However, the underlying mechanisms of kin discrimination are assumed to vary between species and—within species—between contexts. During solitary life stages, kin recognition based on social learning is assumed to be less reliable because kin templates that are not continuously updated may get lost. Therefore, self-referent phenotype matching (“armpit effect”), i.e., the comparison of unknown phenotypes with own characteristics, should be particularly relevant when no social cues are available. However, experimental evidence for this mechanism is scarce. Here, we examine self-referent kin recognition in a mate-choice context in adult male Pelvicachromis taeniatus, a socially monogamous cichlid fish from West Africa with biparental brood care and pronounced kin-mating preferences. Juvenile P. taeniatus live in groups, whereas adult males compete for access to breeding sites which they aggressively defend against rivals. Using computer-animated females as standardized visual stimuli in combination with olfactory cues of related and unrelated females, we show that adult males reared isolated from kin since egg stage were able to discriminate sisters from unrelated females. As males could have learned kin cues only from themselves, our study provides evidence for self-referent kin recognition and indicates that the observed inbreeding preferences are mediated by self-derived olfactory cues. Male preferences for sisters were correlated with male body size. We discuss the implications of quality-related mate choice for the evolution of kin-mating preferences.

Mechanisms of kin discrimination inferred from pedigrees and the spatial distribution of mates

Where animals avoid inbreeding, different mechanisms of kin discrimination can leave different 'signatures' in the patterns of observed mate relationship. For example, consider a species with no paternal care. If a female avoids mating with familiar individuals, one would expect a deficit of offspring whose parents are maternal half-siblings, but paternal half-siblings would be unfamiliar with each other and thus have offspring at the frequency expected by chance. If spatial cues are used to avoid inbreeding, a female would be expected to produce few offspring with males (even unrelated males) living near her birth site. We searched for these and other signatures with data from a long-term study of banner-tailed kangaroo rats, Dipodomys spectabilis, in Arizona, USA, using a combination of intensive censusing, mapping of available dens, microsatellite-based parentage determination, and a randomization routine that determines the numbers of offspring expected if females in the population mate indiscriminately among the males available to them. The data are consistent with the hypothesis that kangaroo rats discriminate kin by familiarity developed via association early in life, rather than by using spatial cues or self-referential phenotype matching. Our approach should be widely applicable as a means of assessing the degree to which kin discrimination exists (in contexts like nepotism as well as inbreeding avoidance) and in inferring what cues animals use to assess categories of relationship.

Message ‘scent’: lemurs detect the genetic relatedness and quality of conspecifics via olfactory cues

To enhance the fitness benefits of social and sexual interaction, animals should be able to decipher information about the genetic makeup of conspecifics. The use of relative criteria to estimate genetic relatedness could facilitate nepotism or inbreeding avoidance, and the use of absolute criteria to estimate genetic quality could help identify the fittest competitor or the best mate. For animals to process trade-offs between relatedness and quality, however, both relative and absolute genetic information must be concurrently available and detectable by conspecifics. Although there is increasing evidence to suggest that animals make genetically informed decisions about their partners, and may even process trade-offs, we understand relatively little about the sensory mechanisms informing these decisions. In previous analyses of the olfactory signals of ringtailed lemurs, Lemur catta, we showed that both scrotal and labial secretions seasonally encode chemical information about (1) pairwise genetic relatedness, within and between the sexes, and (2) individual heterozygosity. Here, using a signaller–receiver paradigm, we conducted behavioural bioassays to test whether male and female lemurs are sensitive to these olfactory sources of genetic information in unfamiliar conspecifics. As the lemurs discriminated conspecific glandular secretions by pairwise relatedness and individual heterozygosity, volatile olfactory signals can be used by both sexes to concurrently process relative and absolute genetic information about conspecifics. Beyond supporting an olfactory mechanism of kin discrimination and mate choice in a primate, we suggest that animals could use olfactory processing to trade off between selection for the most compatible partner versus the most genetically diverse partner.

Polymorphic Members of the lag Gene Family Mediate Kin Discrimination in Dictyostelium

Self and kin discrimination are observed in most kingdoms of life and are mediated by highly polymorphic plasma membrane proteins. Sequence polymorphism, which is essential for effective recognition, is maintained by balancing selection. Dictyostelium discoideum are social amoebas that propagate as unicellular organisms but aggregate upon starvation and form fruiting bodies with viable spores and dead stalk cells. Aggregative development exposes Dictyostelium to the perils of chimerism, including cheating, which raises questions about how the victims survive in nature and how social cooperation persists. Dictyostelids can minimize the cost of chimerism by preferential cooperation with kin, but the mechanisms of kin discrimination are largely unknown. Dictyostelium lag genes encode transmembrane proteins with multiple immunoglobulin (Ig) repeats that participate in cell adhesion and signaling. Here, we describe their role in kin discrimination. We show that lagB1 and lagC1 are highly polymorphic in natural populations and that their sequence dissimilarity correlates well with wild-strain segregation. Deleting lagB1 and lagC1 results in strain segregation in chimeras with wild-type cells, whereas elimination of the nearly invariant homolog lagD1 has no such consequences. These findings reveal an early evolutionary origin of kin discrimination and provide insight into the mechanism of social recognition and immunity.

Social Evolution: The Decline and Fall of Genetic Kin Recognition

Animals should benefit from the ability to recognise their kin, yet curiously this faculty is often absent. New theory confirms that genetic kin recognition is inherently unstable, explaining its rarity.

Is Sociality Driven by the Costs of Dispersal or the Benefits of Philopatry? A Role for Kin‐Discrimination Mechanisms

The role of ecological constraints in promoting sociality is currently much debated. Using a direct-fitness approach, we show this role to depend on the kin-discrimination mechanisms underlying social interactions. Altruism cannot evolve under spatially based discrimination, unless ecological constraints prevent complete dispersal. Increasing constraints enhances both the proportion of philopatric (and thereby altruistic) individuals and the level of altruistic investments conceded in pairwise interactions. Familiarity-based discrimination, by contrast, allows philopatry and altruism to evolve at significant levels even in the absence of ecological constraints. Increasing constraints further enhances the proportion of philopatric (and thereby altruistic) individuals but not the level of altruism conceded. Ecological constraints are thus more likely to affect social evolution in species in which restricted cognitive abilities, large group size, and/or limited period of associative learning force investments to be made on the basis of spatial cues.

The mechanisms of kin discrimination and the evolution of kin recognition in vertebrates: a critical re-evaluation

I re-examine the four most widely proposed mechanisms of kin discrimination among vertebrates and conclude that the current categorization of kin discrimination mechanisms has been counterproductive because it has a hindered a clear understanding of the basic mechanisms by which animals discriminate kin. I suggest that there likely is only one authentic mechanism of kin discrimination and that this mechanism is learning, particularly associative learning and habituation. Observed differences in the way animals discriminate between kin and non-kin are due only to the cues (e.g., individually-distinctive, family-distinctive, or self) that are used, and not to different mechanisms per se. I also consider whether kin discrimination is mediated by specially evolved kin recognition systems, defined as neural mechanisms that allow animals to directly classify conspecifics as either kin or non-kin. A preliminary analysis of vertebrate recognition systems suggests that specialized neural, endocrine, and developmental mechanisms specifically for recognizing kin have not evolved. Rather, kin discrimination results from an extension of other, non-specialized sensory and cognitive abilities of animals, and may be derived from other forms of social recognition, such as individual, group, or species recognition.

Is Sociality Driven by the Costs of Dispersal or the Benefits of Philopatry? A Role for Kin-Discrimination Mechanisms

Is Sociality Driven by the Costs of Dispersal or the Benefits of Philopatry? A Role for Kin-Discrimination Mechanisms

Kin recognition: function and mechanism in avian societies

Cooperative behaviour resulting from kin selection is widespread among animals and the ability to recognize and discriminate between kin and non-kin is a critical element in kin selection theory. Current evidence suggests that associative learning is the most likely mechanism of kin discrimination. However, surprisingly, there have been no experimental studies of the putative ‘associative-learning period', the likely recognition mechanisms enabling fine discrimination between close and distant kin of similar familiarity, whether generic or individual cues are employed in kin recognition, and how recognition ability varies at different stages of a species' life history. Comparative studies of kin recognition and discrimination in cooperative and noncooperative species are also needed to shed light on the adaptive value of helping behaviour and to identify key factors in the evolution of cooperation.

Proximate and ultimate causes of adoption in ring-billed gulls

From 1987 to 1994, the annual frequency of adoption by breeding pairs at a Lake Erie ring-billed gull,Larus delawarensis, colony ranged from 3 to 37% (average 8%/year,N=7 years) and, on average, foster parents raised 0.5 fewer of their own chicks to fledging than pairs that did not adopt. The key evolutionary question is: why do some individuals apparently suffer the costs associated with a behaviour that appears to enhance the fitness of others? From 1992 to 1995, I investigated the proximate and ultimate causes of adoption in ring-billed gulls from the perspectives of both the foster parents and adopted chicks, and tested predictions that differentiated between various competing adaptive and nonadaptive hypotheses that have been proposed to explain it. While I was able to demonstrate a breeding cost, I failed to identify any benefits to foster parents. Thus, the adaptive hypotheses that rely on the foster parents benefiting were not supported (e.g. kin selection, reciprocal altruism, acquisition of parenting experience). From the foster parent’s perspective, adoption was mediated through errors in parent–offspring recognition. Under natural conditions, most fostering pairs were tending small chicks (<6 days old) at the time of adoptions; in chick-transfer experiments, resident parents did not discriminate against foreign chicks until their own chicks were 7–9 days old. Chicks (N=25) that subsequently abandoned their natal nests were lighter, and grew at a slower rate, than chicks that survived to fledging in their home broods. Thus, departing chicks were at a survival disadvantage in their home broods. Chicks that gained acceptance into foreign broods where they were older/larger than the resident chicks realized high survival at the expense of their foster siblings and parents. Based upon individual growth rates and the corresponding survival probabilities, disadvantaged chicks approximately doubled their survival chances through foster care. Why has selection not eliminated adoption? I argue that adoption is an evolutionary arms race between the two principle actor groups; disadvantaged chicks, which benefit through foster care, and host parents, which avoid providing foster care (e.g. infanticide). In ring-billed gulls, selection has failed to eliminate adoption because the long-term reproductive cost (estimated at 4%, this study) of an occasional adoption is probably offset by the relatively higher costs associated with stricter kin discrimination mechanisms (e.g. parental infanticide).

Why do male birds not discriminate between their own and extra-pair offspring?

A number of recent models of optimal paternal investment predict that males should alter their investment in offspring in response to changes in paternity or certainty of paternity. One way in which it has been suggested that male birds might do this would be to recognize their own offspring and to discriminate in their favour. Despite frequent statements that nothing is known about whether birds possess this ability or whether they exercise it, there is a considerable body of evidence suggesting that males do not discriminate against non-related offspring. This evidence is reviewed and an attempt made to explain the absence of kin discrimination in males under these circumstances by considering potential mechanisms of kin discrimination. Although there is selection for males to discriminate in favour of their own offspring it is argued that they are unable to do so because of conflicts between the male, female and offspring over signalling identity, and because the circumstances associated with extra-pair paternity disrupt the operation of some mechanisms. Male birds might possess behavioural ‘rules of thumb’ which lead to behaviour that appears similar to offspring recognition, but the sophistication of such rules is likely to be limited by the stochasticity inherent in fertilization.

Primate mating systems, kin associations, and cooperative behavior: Evidence for kin recognition?

The degree to which cooperative behavior is kin-correlated in different primate species is reviewed. The mechanisms whereby individuals might recognize related conspecifics are also considered. Different mating systems, in conjunction with dispersal behavior, are hypothesized to produce particular patterns of kin association in primate groups. These patterns determine what classes of kin are likely to be distinguished, as well as which mechanisms of recognition would be predicted. Association or familiarity during development is concluded to be the most important mechanism of kin discrimination in the primates.