“KIN RECOGNITION” AMONG SPADEFOOT TOAD TADPOLES: A SIDE-EFFECT OF HABITAT SELECTION?

Many animals modify their behavior toward unfamiliar conspecifics as a function of their genetic relatedness. A fundamental problem of any kin recognition study is determining what is being recognized and why. For anuran tadpoles, the predominant view is that associating with relatives is kin-selected because these relatives may thereby accrue benefits through increased growth or predation avoidance. An alternative view is that kin associations are simply a side-effect of habitat selection and thus do not represent attempts to identify kin per se. In the laboratory, spadefoot toad tadpoles (Scaphiopus multiplicatus) preferentially associated with unfamiliar siblings over unfamiliar nonsiblings, as do other anurans. However, same age tadpoles also were more likely to orient toward unfamiliar nonsiblings reared on the same food (familiar food) than toward unfamiliar siblings that were reared on unfamiliar food. These results, together with the results of previous tadpole kin recognition studies, suggest that tadpoles orient toward cues learned early in ontogeny, regardless of the cues' source. Tadpoles that preferentially associated with cues learned from their environment at birth would tend to be philopatric. Censuses of 14 natural ponds revealed that tadpole density remained greatest near oviposition sites until four days before metamorphosis. Tadpole philopatry may be advantageous: tadpoles restricted to their natal site had greater growth and survivorship than did their siblings restricted to randomly selected sites elsewhere within the same pond. Thus kin affiliative tendency observed in the laboratory in this and perhaps other species of anurans may be a byproduct of habitat selection. Since kin discrimination in animals is most commonly assayed as orientation toward kin, it follows that many examples of “kin recognition” may not represent true attempts to identify kin as such, but rather may reflect some other recognition system that is under entirely different selective pressures.     

Rana cascadae tadpoles aggregate with siblings: an experimental field study

Previous laboratory studies have shown that Rana cascadae larvae preferentially associated with siblings over non-siblings in choice tests. This study, conducted during three consecutive summers, tests the hypothesis that R. cascadae larvae aggregate nonrandomly with respect to sibship in natural ponds. Pairs of sibships were reared in separate tanks or together in the same tank in the laboratory. Each sibship within a pair was then stained with neutral red or methylene blue dye and released together in a natural pond. Over a period of several days, aggregations of tadpoles within test ponds were repeatedly captured, censused for sibship composition, and released. In control tests, two groups of tadpoles from the same sibship were dyed different colors and released together. In total, 25 different tests were conducted using tadpoles from 31 sibships and 456 aggregations were sampled. The distribution of color compositions of aggregations in control tests did not differ from an expected random distribution. Color compositions of aggregations in experimental tests differed from controls and from an expected random distribution. Aggregations in these tests tended to be dominated by one of the two colors (sibships). We conclude that R. cascadae tadpoles recognize and prefer to aggregate with siblings in natural field conditions. Circumstances of early rearing (i.e., whether tadpoles were reared with siblings or in mixed sibling/non-sibling groups) had no influence on preferences to associate with siblings, but there was an inverse correlation between group size and sibling association.     

植物的亲缘选择

亲缘选择是指在一个随机交配群体中的个体基于亲缘关系而以一种非随机性的方式相互作用,其作用结果是亲缘个体得到更大的广义适合度。综述了亲缘选择和亲缘竞争两种观点以及各自的试验支持证据;分析了导致亲缘选择试验结果出现分歧的原因,认为这主要是由于对亲缘选择理解上的模糊以及试验设计的不严谨所致。植物间的亲缘选择研究不仅相对较少,对亲缘选择的机制研究更为欠缺,这就造成了目前对此问题在科学认识上出现不少盲点。综合前期研究,提出今后对亲缘选择的研究应该首先界定"亲缘"程度,同时改良试验设计方案,选择多种不同生境下的物种对亲缘选择进行深入研究,并且考虑环境因子对植物亲缘选择的影响。同时,对植物亲缘识别机制的研究应该从生理生化方面出发,通过定性定量地分析探索植物根系分泌物在植物亲缘识别中的作用和作用途径。     

Relatedness and resource diversity interact to influence the intensity of competition

When resource competition occurs between close relatives, the negative effects of competition are potentially amplified. However, kin selection theory predicts that natural selection should promote the evolution of mechanisms that minimize the intensity of competition between kin. Experimental tests of these hypotheses are mixed, however. Moreover, there is little consensus regarding the generality of either outcome, suggesting that the conditions important in determining the effects of competition between kin are likely complex and not fully understood. We performed two experiments using spadefoot toad tadpoles (Spea multiplicata) to evaluate the hypothesis that individuals can minimize the negative effects of exploitative competition by using alternative resources when competing with close relatives. Supporting our hypothesis, we found that only when individuals had access to alternative resources were the negative effects of competition between siblings less than between unrelated competitors. We suggest that mechanisms to lessen kin competition may be more likely to evolve in environments where alternative resources are available, and that selection to minimize exploitative competition between kin may promote the evolution of resource polyphenism. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 689–695.     

A test of alternative hypotheses for kin recognition in cannibalistic tiger salamanders

The function of kin recognition is controversial. We investigatedthe adaptive significance of kin discrimination in cannibalistictiger salamander larvae, Ambystoma tigrinum. Previous laboratoryexperiments show that cannibals preferentially consume lessrelated individuals. We hypothesized that this example of kinrecognition (1) is a laboratory artifact, (2) is a by-productof sibship-specific variation in escape responses, because cannibalsfrom families with rapid responses may be more likely to cannibalize slowlyescaping non-kin, (3) is an epiphenomenon of species recognition,(4) functions in disease avoidance, because kin may be moreinfectious than non-kin, or (5) is favored by kin selection.We evaluated these five hypotheses by using laboratory and fieldexperiments to test specific predictions made by each hypothesis.We rejected hypotheses 1-4 above because (1) kin recognitionwas expressed in the wild, (2) escape responses did not reliablypredict whether a cannibal would ingest kin or non-kin, (3)kin recognition was not most pronounced in populations wheretiger salamanders co-occur with other species of salamanders,and (4) non-kin prey were more likely than kin to transmit pathogensto cannibals. However, we established that the necessary conditionfor kin selection, Hamilton's rule, was met. Thus, our resultsimplicate kin selection as the overriding reason that cannibalistictiger salamanders discriminate kin.     

The cost of aggregation: juvenile salmon avoid sharing winter refuges with siblings

Kin selection advantages are usually accrued by individualsthat associate with close relatives. But aggregation may alsobe costly, by increasing the risk of predation or resource competition,for example. As a result, individuals should increase theirinclusive fitness by trading the costs and benefits of kin associationand aggregation. Studies of kin selection to date have focusedon situations where there is ample opportunity for kin-biasedbehavior and therefore for the formation of kin groups. Herewe used juvenile Atlantic salmon to test an alternative strategy:that under conditions where the potential for kin-biased behavioris negligible, individuals should, when aggregating, avoid ratherthan associate with kin to avoid imposing the costs of aggregationupon close relatives. By testing salmon during winter, whenjuveniles shelter inactively in streambed refuges, we testedwhether individuals associate with or avoid their siblings ata time when the opportunity for kin-directed behaviors is restricted.Our results provide the first evidence of kin avoidance in nonreproductiveanimals studied under semi-natural conditions.     

Carnivory and resource-based niche differentiation in anuran larvae: implications for food web and experimental ecology

1.  Food webs represent the paths of material and energy flow through organisms in an ecosystem. Anuran larvae are important components of pond food webs: they are abundant, consume large quantities of food and serve as prey for many organisms. However, there are very basic uncertainties about the feeding ecology of anuran larvae; for instance, as to which trophic level they belong and whether species differ in resource use. Because anuran larvae have been employed in model systems in experimental ecology for decades, these uncertainties could lead to misinterpretation of published experiments, or inadequate designs of experiments directed at general, conceptual issues in ecology.
2.  Using ¹³C and ¹⁵N stable isotope and gut content analyses of free-ranging and enclosed tadpoles of four ranid species ( Lithobates sylvaticus , L. pipiens , L. clamitans , L. catesbeianus ) in the food webs of six wetlands, we tested the following null hypotheses: (i) that anuran larvae are strict primary consumers; (ii) that they are non-selective feeders and therefore exhibit little feeding niche differentiation; (iii) that they are opportunistic consumers and (iv) that their diet remains unchanged through ontogeny.
3.  All four species consumed and assimilated substantial amounts of animal food; bullfrog larvae, in particular, appear to be predatory. Significant feeding niche differentiation among species occurred with respect to the sources of carbon, consumption of animal matter and nutritional quality of food ingested. We further documented opportunistic feeding habits and ontogenetic shifts in diet.
4.  Collectively, these studies revealed complex trophic relationships that might require a reconsideration of the role of anuran larvae in pond food webs, as well as a reinterpretation of results of previous studies employing anuran larvae in model experimental systems.     

The ontogeny of kin recognition in tadpoles of the toadBufo melanostictus (Anura; Bufonidae)

The ontogeny of kin recognition and influence of social environment on the development of kin recognition behaviour was experimentally investigated in tadpoles of Bufo melanostictus that lived in aggregations and showed low larval dispersion. Embryos and tadpoles of the toad were reared as (i) kin only, (ii) with kin and non-kin (separated by a mesh screen), and (iii) in isolation. They were tested for the ability to discriminate between (i) familiar siblings and unfamiliar non-siblings, (ii) familiar siblings and familiar non-siblings and, (iii) unfamiliar siblings and unfamiliar non-siblings. All tadpoles were fed on boiled spinach before conducting trials. Preference of test tadpoles to associate near the end compartments whether empty or containing members of specific stimulus groups was assessed using a rectangular choice tank. When tested in tanks with empty end compartments, the test tadpoles showed random distribution and thus no bias for the apparatus or the procedure. In the presence of kin/non-kin in the end compartments a significantly greater number of test tadpoles spent the majority of the time near familiar or unfamiliar kin rather than near familiar or unfamiliar non-kin. Kin discrimination ability persisted throughout larval development. Familiarity with siblings is not required for discriminating kin from non-kin, and kin discrimination ability is not modified following exposure to non-kin. Also, involvement of dietary cues is unlikely to be the prime mechanism of kin recognition inB. melanostictus unlike in some other anurans.     

Association preference and mechanism of kin recognition in tadpoles of the toad <Emphasis Type="Italic">Bufo melanostictus</Emphasis>

In experiments with specially designed choice tanks, tadpoles of Bufo melanostictus spend significantly greater amounts of time near kin than near non-kin. However, in the absence of kin members, they prefer to spend more time near non-kin rather than stay away in isolation in the opposite blank zone with no company. This implies that association of toad tadpoles with their kin is due to attraction rather than repulsion from non-kin. Experiments designed to elucidate the sensory basis of kin recognition showed that toad tadpoles recognize their kin based on chemical cues rather than visual cues. They can also discriminate between homospecific non-kin and heterospecific (Sphaerotheca breviceps) tadpoles since the tadpoles spent significantly greater amounts of time near the former than near the latter. These findings suggest that where kin members are unavailable, selection may have favoured living with non-kin so as to derive benefits from group living and that a phenotype-matching mechanism may operate for both kin and species discrimination in B. melanostictus.     

Paternal kin discrimination: the evidence and likely mechanisms

One of the most important assumptions of kin selection theory is that individuals behave differently towards kin than non-kin. In mammals, there is strong evidence that maternal kin are distinguished from non-kin via familiarity. However, little is known about whether or not mammals can also recognize paternal kin as many female mammals, including primates, mate with multiple males near the time of conception, potentially concealing paternal kinship. Genetic data in several mammalian species with a promiscuous mating system and male-biased dispersal reveal a high skew in male reproduction which leads to co-residing paternal half-siblings. In most primates, individuals also form stable bisexual groups creating opportunities for males to interact with their offspring. Here I consider close paternal kin co-resident in the same social group, such as father-offspring and paternal half-siblings (i.e. animals sharing the same father but who were born to different mothers) and review mammalian studies of paternal kin discrimination. Furthermore, I summarize the most likely mechanisms of paternal kin discrimination (familiarity and phenotype matching). When familiarity is the underlying mechanism, mothers and/or the sire could mediate familiarity among paternal half-siblings as well as between fathers and offspring assuming mothers and/or fathers can assess paternity. When animals use phenotype matching, they might use their fathers' template (when the father is present) or self (when the father is absent) to assess paternal kinship in others. Available evidence suggests that familiarity and phenotype matching might be used for paternal kin discrimination and that both mechanisms might apply to a wide range of social mammals characterized by a high skew in male reproduction and co-residence of paternal kin. Among primates, suggested evidence for phenotype matching can often have an alternative explanation, which emphasizes the crucial importance of controlling for familiarity as a potential confounding variable. However, the mechanism/s used to identify paternal kin might differ within a species (as a function of each individual's specific circumstances) as well as among species (depending upon the key sensory modalities of the species considered). Finally, I discuss the possible cues used in paternal kin discrimination and offer suggestions for future studies.     

Kin recognition in Bufo scaber tadpoles: ontogenetic changes and mechanism

Ontogenetic changes in kin-recognition behavior, effect of social environment on kin-recognition ability, and use of visual and chemical cues in kin recognition have been studied in tadpoles of Bufo scaber after rearing them with kin, in mixed groups, or in isolation from Gosner stage 12 (gastrula). By use of a rectangular choice tank the tadpoles were tested for their ability to choose between (a) familiar siblings and unfamiliar non-siblings, (b) unfamiliar siblings and familiar non-siblings, and (c) unfamiliar siblings and unfamiliar non-siblings. When tested without any stimulus groups in the end compartments of the tank, random distribution was observed for the tadpoles and no bias for the apparatus or the procedure. In the presence of kin and non-kin in the end compartments, significantly more tadpoles spent most of their time near kin (familiar or unfamiliar) rather than near non-kin during early larval stages, up to stage 37. After stage 37 (characterized by the differentiation of toes), test tadpoles showed no preference to associate with kin, suggesting an ontogenetic shift in the kin-recognition ability in B. scaber. In experiments involving selective blockade of visual or chemical cues the test tadpoles preferentially associated near their kin on the basis of chemical rather than visual cues. These findings suggest that familiarity with siblings is not necessary for kin recognition and that kin-recognition ability is not modified after exposure to non-kin by mixed rearing. The findings for B. scaber indicate a self referent phenotype matching mechanism of kin recognition which is predominantly aided by chemical rather than visual cues.     

KIN-MEDIATED MORPHOGENESIS IN FACULTATIVELY CANNIBALISTIC TADPOLES

Inclusive fitness theory predicts that organisms can increase their fitness by helping or not harming relatives, and many animals modify their behavior toward kin in a manner consistent with this prediction. Morphogenesis also may be sensitive to kinship environment, particularly in species where certain individuals facultatively develop structures that can be used against conspecifics as weaponry. We tested this hypothesis by examining whether and how consanguinity affected the probability that a structurally distinctive carnivore phenotype, which is opportunistically cannibalistic, would be produced in plains spadefoot toad tadpoles (Spea bombifrons) and southern spadefoot toad tadpoles (S. multiplicata). For tadpoles of S. multiplicata, individuals were significantly more likely to express the carnivore phenotype in mixed sibship groups than in pure sibship groups. For tadpoles of S. bombifrons, individuals were significantly more likely to express the carnivore phenotype when reared alone than in pure sibship groups. Both outcomes were independent of food availability or sibship specific differences in size or growth rate, and waterborne chemical signals from nonkin were sufficient to trigger expression of the carnivore phenotype. Our results suggest that morphogenesis may be responsive to kinship environment in any species or population that occurs as multiple, environmentally induced forms (polyphenism) that differ in their ability to help or to harm others.     

Growing with siblings: a common ground for cooperation or for fiercer competition among plants?

Recent work has shown that certain plants can identify their kin in competitive settings through root recognition, and react by decreasing root growth when competing with relatives. Although this may be a necessary step in kin selection, no clear associated improvement in individual or group fitness has been reported to qualify as such. We designed an experiment to address whether genetic relatedness between neighbouring plants affects individual or group fitness in artificial populations. Seeds of Lupinus angustifolius were sown in groups of siblings, groups of different genotypes from the same population and groups of genotypes from different populations. Both plants surrounded by siblings and by genotypes from the same population had lower individual fitness and produced fewer flowers and less vegetative biomass as a group. We conclude that genetic relatedness entails decreased individual and group fitness in L. angustifolius. This, together with earlier work, precludes the generalization that kin recognition may act as a widespread, major microevolutionary mechanism in plants.     

Limited indirect fitness benefits of male group membership in a lekking species

In group living species, individuals may gain the indirect fitness benefits characterizing kin selection when groups contain close relatives. However, tests of kin selection have primarily focused on cooperatively breeding and eusocial species, whereas its importance in other forms of group living remains to be fully understood. Lekking is a form of grouping where males display on small aggregated territories, which females then visit to mate. As females prefer larger aggregations, territorial males might gain indirect fitness benefits if their presence increases the fitness of close relatives. Previous studies have tested specific predictions of kin selection models using measures such as group‐level relatedness. However, a full understanding of the contribution of kin selection in the evolution of group living requires estimating individuals' indirect fitness benefits across multiple sites and years. Using behavioural and genetic data from the black grouse (Tetrao tetrix), we show that the indirect fitness benefits of group membership were very small because newcomers joined leks containing few close relatives who had limited mating success. Males' indirect fitness benefits were higher in yearlings during increasing population density but marginally changed the variation in male mating success. Kin selection acting through increasing group size is therefore unlikely to contribute substantially to the evolution and maintenance of lekking in this black grouse population.     

Direct and indirect effects of the introduced toad Bufo marinus (Anura: Bufonidae) on populations of native anuran larvae in Australia

Introduced species are frequently believed to have adverse effects on native biota and ecosystems. However, much of our knowledge of the ecological impacts of introduced species is anecdotal, and the mechanisms controlling these effects are often poorly understood. I used replicated artificial pond experiments to investigate the impact of eggs and hatchlings of the introduced toad Bufo marinus on populations of native anuran larvae (Limnodynastes ornatus and Litoria rubella) in Australia. Bufo marinus eggs and hatchlings are highly toxic to predatory native tadpoles. Under naturalistic conditions, populations of predatory L. ornatus tadpoles experienced significantly reduced survival when exposed to Bufo eggs and hatchlings. The impact of Bufo on L. ornatus survival was positively correlated with Bufo density. However, the toxic effects of Bufo on L. ornatus indirectly facilitated the survival of later-breeding L. rubella by altering predator-prey interactions between L. ornatus and L. rubella. Limnodynastes ornatus tadpoles are voracious predators of L. rubella eggs and hatchlings. Consequently, the negative impact of Bufo on populations of L. ornatus tadpoles reduced the intensity of predation by L. ornatus tadpoles on L. rubella eggs and hatchlings, thereby increasing L. rubella survival. The results demonstrate that B. marinus plays an important role in structuring native larval anuran communities via direct and indirect mechanisms, and that Bufo may have both negative and positive effects on populations of native anuran larvae. As far as I am aware, these are the first quantitative data to demonstrate that introduced fauna may affect populations of native biota via toxic effects.     

Kin recognition by paternal half-siblings in captive Papio cynocephalus

Our objective in this study was to evaluate whether a group of paternally related, subadult baboons (Papio cynocephalus) would preferentially interact with kin or nonkin when they had been raised apart from kin other than their mothers. Subjects and their mothers were removed from the breeding group and placed in alternate housing within 24 h after birth to ensure that the subjects would not have a social history with either their sire or their half-siblings. At 90 days of age, the 23 subjects were separated from their mothers and assigned to a peer–peer social group. Behavioral performance was measured using focal animal sampling techniques and 12 molecular behavioral criteria. Analyses of the data indicate that in dyadic interactions kin did not interact more frequently than nonkin in performance of affiliative, sociosexual, and agonistic behaviors. The hypothesis that baboons recognize kin in the absence of maternal associations was not supported by the data; moreover, we suggest that social learning and social history are the most likely mechanisms for kin recognition. Am. J. Primatol. 43:147–157, 1997. © 1997 Wiley-Liss, Inc.     

Do male moor frogs (Rana arvalis) lek with kin?

Many amphibian species are known to form leks during breeding season, yet it has seldom been tested which evolutionary forces are likely to act on lek formation in this taxon. We tested the kin selection hypothesis for lek formation by using eight variable microsatellite loci to compare the genetic relationship of 203 males in seven Rana arvalis leks. The results indicate that moor frog males do not lek with kin: their relatedness within leks was not higher than expected by chance. Furthermore, spatially distinct leks within same water bodies could not be distinguished from each other as separate units. These results are not expected if kin selection underlie lek formation. On the basis of these results and general knowledge of anuran breeding biology, we suggest that lek formation in explosively breeding amphibians might have evolved by female choice for breeding aggregations, combined with female choice of habitat. Future work should aim at predicting aggregations based on rules of phonotaxis over different spatial scales, and empirical work should document visitation rates not only for leks of a specific size, but also for different travel distances that visiting females may have had to cover.     

Recent advance of kin recognition in plant

Plants have the ability to discriminate kin members from strangers in competitive interactions and show altruistic behavior towards related individuals. Studies have showed that plants recognize their neighbors and adjust their ecological strategy mainly through leaf volatiles, root secretions and photographic carrier. The target plants can modify their morphological traits (root size, root:shoot ratio, seed numbers etc.) or metabolism characteristics (secondary metabolites, defense-related proteins etc.) when groups of plants shared common resources, so as to minimize competition with close relatives. The density of kin recognition is influenced by environmental conditions. The main reasons for controversial experimental results of kin recognition are associated with plant materials, standard of kin selection, ecological factors and measured indices. Further studies are required to understand the mechanisms of kin interactions in plants from physiological, biochemical, molecular and metabolic levels.     

Kin Selection in Primate Groups

Altruism poses a problem for evolutionary biologists because natural selection is not expected to favor behaviors that are beneficial to recipients, but costly to actors. The theory of kin selection, first articulated by Hamilton (1964), provides a solution to the problem. Hamilton's well-known rule (br > c) provides a simple algorithm for the evolution of altruism via kin selection. Because kin recognition is a crucial requirement of kin selection, it is important to know whether and how primates can recognize their relatives. While conventional wisdom has been that primates can recognize maternal kin, but not paternal kin, this view is being challenged by new findings. The ability to recognize kin implies that kin selection may shape altruistic behavior in primate groups. I focus on two cases in which kin selection is tightly woven into the fabric of social life. For female baboons, macaques, and vervets maternal kinship is an important axis of social networks, coalitionary activity, and dominance relationships. Detailed studies of the patterning of altruistic interactions within these species illustrate the extent and limits of nepotism in their social lives. Carefully integrated analyses of behavior, demography, and genetics among red howlers provide an independent example of how kin selection shapes social organization and behavior. In red howlers, kin bonds shape the life histories and reproductive performance of both males and female. The two cases demonstrate that kin selection can be a powerful source of altruistic activity within primate groups. However, to fully assess the role of kin selection in primate groups, we need more information about the effects of kinship on the patterning of behavior across the Primates and accurate information about paternal kin relationships.     

Fine‐scale genetic structure and helping decisions in a cooperatively breeding bird

In animal societies, characteristic demographic and dispersal patterns may lead to genetic structuring of populations, generating the potential for kin selection to operate. However, even in genetically structured populations, social interactions may still require kin discrimination for cooperative behaviour to be directed towards relatives. Here, we use molecular genetics and long‐term field data to investigate genetic structure in an adult population of long‐tailed tits Aegithalos caudatus, a cooperative breeder in which helping occurs within extended kin networks, and relate this to patterns of helping with respect to kinship. Spatial autocorrelation analyses reveal fine‐scale genetic structure within our population, such that related adults of either sex are spatially clustered following natal dispersal, with relatedness among nearby males higher than that among nearby females, as predicted by observations of male‐biased philopatry. This kin structure creates opportunities for failed breeders to gain indirect fitness benefits via redirected helping, but crucially, most close neighbours of failed breeders are unrelated and help is directed towards relatives more often than expected by indiscriminate helping. These findings are consistent with the effective kin discrimination mechanism known to exist in long‐tailed tits and support models identifying kin selection as the driver of cooperation.