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.     

Routes to indirect fitness in cooperatively breeding vertebrates: kin discrimination and limited dispersal

Hamilton demonstrated that the evolution of cooperative behaviour is favoured by high relatedness, which can arise through kin discrimination or limited dispersal (population viscosity). These two processes are likely to operate with limited overlap: kin discrimination is beneficial when variation in relatedness is higher, whereas limited dispersal results in less variable and higher average relatedness, reducing selection for kin discrimination. However, most empirical work on eukaryotes has focused on kin discrimination. To address this bias, we analysed how kin discrimination and limited dispersal interact to shape helping behaviour across cooperatively breeding vertebrates. We show that kin discrimination is greater in species where the: (i) average relatedness in groups is lower and more variable; (ii) effect of helpers on breeders reproductive success is greater; and (iii) probability of helping was measured, rather than the amount of help provided. There was also an interaction between these effects with the correlation between the benefits of helping and kin discrimination being stronger in species with higher variance in relatedness. Overall, our results suggest that kin discrimination provides a route to indirect benefits when relatedness is too variable within groups to favour indiscriminate cooperation.     

Multiple paternity and kin recognition mechanisms in a guppy population

Help directed toward kin (nepotism) is an important example of social behaviour. Such helping behaviour requires a mechanism to distinguish kin from nonkin. The prevailing kin recognition hypothesis is that when familiarity is a reliable cue of relatedness, other mechanisms of recognition will not evolve. However, when familiarity is an unreliable cue of relatedness, kin recognition by phenotype matching is instead predicted to evolve. Here we use genetic markers to show that guppies (Poecilia reticulata) from a population in a tributary of the Paria River in Trinidad are characterized by a high degree of multiple mating with 95% of broods having more than one sire and some dams having offspring sired by six males. These levels of multiple mating are the highest reported among live-bearing fishes. The mean relatedness of brood-mates was 0.36 (as compared to 0.5 for full-siblings). Therefore, familiarity does not seem to be a reliable mechanism to assess full-sibling relatedness. Using two-choice behavioural trials, we found that juveniles from this population use both phenotype matching and familiarity to distinguish kin from nonkin. However, we did not find strong evidence that the guppies use these mechanisms to form shoals of related individuals as adults, which is similar to results from other guppy populations in Trinidad. The use of both familiarity and phenotype matching is discussed in the context of the Paria River guppy population's mating system and ecology. Overall, these data provide support for the kin recognition hypothesis and increase our understanding of the evolution of kin recognition systems.     

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.     

The role of kin recognition in the evolution of conspecific brood parasitism

Conspecific brood parasitism (CBP) is a common strategy in several species of birds. Currently, some studies suggest that relatedness between host and parasite enhances CBP, since indirect fitness benefits could select for acceptance of related eggs by hosts. Conversely, parasites should avoid laying eggs in nests of relatives if this is costly for the host. Based on the latter argument, kinship should not promote brood parasitism. A recent model clarified this relationship, and showed that kinship can promote brood parasitism, assuming kin recognition. However, in that model kin recognition was assumed perfect. Here we present a model that addresses the role of relatedness and kin selection in CBP, when kin recognition is not perfect and hosts do not always detect parasitism. We consider both the indirect fitness of the parasite and the possible responses of the host. Our results indicate that the existence and accuracy of a kin recognition system is crucial to the final outcome. When CBP represents a cost to the host, a parasitic female that has the choice should avoid parasitizing relatives, unless (1) the costs are not too high and (2) hosts can accurately enough recognize eggs laid by relatives, rejecting them less often than eggs laid by nonkin. But if ‘parasitism’ enhances the direct fitness of the host (which is possible in species with precocial young) parasites should choose relatives whenever possible, even if hosts do not recognize kin eggs. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Innate visual object recognition in vertebrates: some proposed pathways and mechanisms

Almost all vertebrates are capable of recognizing biologically relevant stimuli at or shortly after birth, and in some phylogenetically ancient species visual object recognition is exclusively innate. Extensive and detailed studies of the anuran visual system have resulted in the determination of the neural structures and pathways involved in innate prey and predator recognition in these species [Behav. Brain Sci. 10 (1987) 337; Comp. Biochem. Physiol. A 128 (2001) 417]. The structures involved include the optic tectum, pretectal nuclei and an area within the mesencephalic tegmentum. Here we investigate the structures and pathways involved in innate stimulus recognition in avian, rodent and primate species. We discuss innate stimulus preferences in maternal imprinting in chicks and argue that these preferences are due to innate visual recognition of conspecifics, entirely mediated by subtelencephalic structures. In rodent species, brainstem structures largely homologous to the components of the anuran subcortical visual system mediate innate visual object recognition. The primary components of the mammalian subcortical visual system are the superior colliculus, nucleus of the optic tract, anterior and posterior pretectal nuclei, nucleus of the posterior commissure, and an area within the mesopontine reticular formation that includes parts of the cuneiform, subcuneiform and pedunculopontine nuclei. We argue that in rodent species the innate sensory recognition systems function throughout ontogeny, acting in parallel with cortical sensory and recognition systems. In primates the structures involved in innate stimulus recognition are essentially the same as those in rodents, but overt innate recognition is only present in very early ontogeny, and after a transition period gives way to learned object recognition mediated by cortical structures. After the transition period, primate subcortical sensory systems still function to provide implicit innate stimulus recognition, and this recognition can still generate orienting, neuroendocrine and emotional responses to biologically relevant stimuli.     

Absence of kin discrimination in a ponerine ant

Kinship theory implies that individual social Hymenoptera should be able to identify kin. We tested kin discrimination in the polygynous ponerine ant Gnamptogenys striatula. Mate choice experiments showed that individuals did not pair according to kinship. Experiments on matriline discrimination revealed that workers did not preferentially groom, transport (after nest disturbance) or cannibalize (after starvation) larvae on the basis of kin, when both related and unrelated larvae were present. These results show the absence of kin discrimination for the criteria and experimental conditions used. The lack of kin discrimination during mate choice in G. striatula can be explained by male dispersion and female philopatry, which reduces the likelihood of mating between siblings and of kin-based mate choice reflected in incest avoidance. The lack of matriline discrimination by workers may reflect permanent intracolony mutualism or the high cost of discrimination. Finally, it appears that the absence of kin discrimination in such contexts in G. striatula is not incompatible with kinship theory and may have been secondarily selected during social evolution. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Olfactory kin recognition in a songbird

The ability to recognize close relatives in order to cooperate or to avoid inbreeding is widespread across all taxa. One accepted mechanism for kin recognition in birds is associative learning of visual or acoustic cues. However, how could individuals ever learn to recognize unfamiliar kin? Here, we provide the first evidence for a novel mechanism of kin recognition in birds. Zebra finch (Taeniopygia guttata) fledglings are able to distinguish between kin and non-kin based on olfactory cues alone. Since olfactory cues are likely to be genetically based, this finding establishes a neglected mechanism of kin recognition in birds, particularly in songbirds, with potentially far-reaching consequences for both kin selection and inbreeding avoidance.     

The phyllolepid placoderm Cowralepis mclachlani: Insights into the evolution of feeding mechanisms in jawed vertebrates

Remarkably preserved specimens of Cowralepis mclachlani Ritchie, 2005 (Proc Linn Soc NSW 126:215–259) (Phyllolepida, Placodermi) represent a unique ontogenetic sequence adding to our understanding of anatomy, function, and phylogeny among basal jawed vertebrates (gnathostomes). A systematic review demonstrates that the Phyllolepida are a subgroup of the Arthrodira. Consideration of visceral and neurocranial characters supports the hypothesis that placoderms are the sister group to remaining gnathostomes. Placoderms possess, as adult plesiomorphic features, a number of characters that are only seen in the development of extant gnathostomes—a peramorphic shift relative to placoderms. Developmental evidence in vertebrates leads to a revised polarity of character transitions. These include 1) hyomandibula‐neurocranium and ventral parachordal‐palatoquadrate articulations (vertebrate synapomorphies); 2) jointed pharynx, paired basibranchials, anterior ethmoidal‐palatoquadrate articulation, short trabeculae cranii, and anterior and posterior neurocranial fissures (gnathostome synapomorphies); and 3) fused basibranchials, dorsal palatoquadrate‐neurocranium articulation, loss of the anterior neurocranial fissure, elongated trabeculae cranii, and transfer of the ventral parachordal‐palatoquadrate articulation to the trabeculae (crown group gnathostomes). The level of preservation in C. mclachlani provides the basis for a reinterpretation of phyllolepid anatomy and function. Cowralepis mclachlani possesses paired basibranchials allowing the reinterpretation of the visceral skeleton in other placoderms. Mandible depression in C. mclachlani follows an osteichthyan pattern and the ventral visceral skeleton acts as a functional unit. Evidence for hypobranchial musculature demonstrates the neural crest origin of the basibranchials and that Cowralepis was a suction feeder. Finally, the position of the visceral skeleton relative to the neurocranium in placoderms parallels the condition in selachians and osteichthyans, but differs in the elongation of the occiput. The cucullaris fossa of placoderms (interpreted as a site of muscle attachment) is shown to represent, in part, the parabranchial chamber. J. Morphol., 2009. © 2009 Wiley‐Liss, Inc.     

New perspectives on the evolution of lung ventilation mechanisms in vertebrates

In the traditional view of vertebrate lung ventilation mechanisms, air-breathing fishes and amphibians breathe with a buccal pump, and amniotes breathe with an aspiration pump. According to this view, no extant animal exhibits a mechanism that is intermediate between buccal pumping and aspiration breathing; all lung ventilation is produced either by expansion and compression of the mouth cavity via the associated cranial and hyobranchial musculature (buccal pump), or by expansion of the thorax via axial musculature (aspiration pump). However, recent work has shown that amphibians exhibit an intermediate mechanism, in which axial muscles are used for exhalation and a buccal pump is used for inhalation. These findings indicate that aspiration breathing evolved in two steps: first, from pure buccal pumping to the use of axial musculature for exhalation and a buccal pump for inspiration; and second, to full aspiration breathing, in which axial muscles are used for both inhalation and exhalation. Furthermore, the traditional view also holds that buccal pump breathing was lost shortly after aspiration breathing evolved. This view is now being challenged by the discovery that several species of lizards use a buccal pump to augment costal aspiration during exercise. This result, combined with the observation that a behavior known as “buccal oscillation” is found in all amniotes except for mammals, suggests that a reappraisal of the role of buccal pumping in extant and extinct amniotes is in order.Electronic supplementary material Electronic supplementary material is available for this article at and accessible for authorised users.     

The biogeography of kin discrimination across microbial neighbourhoods

The spatial distribution of potential interactants is critical to social evolution in all cooperative organisms. Yet the biogeography of microbial kin discrimination at the scales most relevant to social interactions is poorly understood. Here we resolve the microbiogeography of social identity and genetic relatedness in local populations of the model cooperative bacterium Myxococcus xanthus at small spatial scales, across which the potential for dispersal is high. Using two criteria of relatedness—colony‐merger compatibility during cooperative motility and DNA‐sequence similarity at highly polymorphic loci—we find that relatedness decreases greatly with spatial distance even across the smallest scale transition. Both social relatedness and genetic relatedness are maximal within individual fruiting bodies at the micrometre scale but are much lower already across adjacent fruiting bodies at the millimetre scale. Genetic relatedness was found to be yet lower among centimetre‐scale samples, whereas social allotype relatedness decreased further only at the metre scale, at and beyond which the probability of social or genetic identity among randomly sampled isolates is effectively zero. Thus, in M. xanthus, high‐relatedness patches form a rich mosaic of diverse social allotypes across fruiting body neighbourhoods at the millimetre scale and beyond. Individuals that migrate even short distances across adjacent groups will frequently encounter allotypic conspecifics and territorial kin discrimination may profoundly influence the spatial dynamics of local migration. Finally, we also found that the phylogenetic scope of intraspecific biogeographic analysis can affect the detection of spatial structure, as some patterns evident in clade‐specific analysis were masked by simultaneous analysis of all strains.     

Genotypic and kin discrimination in a solitary Hymenopterous parasitoid: Implications for speciation

In Hymenopterous parasitoids, host discrimination enables a female to avoid ovipositing in an already parasitized host. A female recognizes such hosts by the presence of external or internal pheromone markings that differ depending on whether the host has been parasitized by the same female, a conspecific or a female of another species. If the ability to recognize hosts parasitized by genetically distant females does exist and results in a change in acceptance, this behaviour would have an impact on sympatric speciation. We tested this hypothesis in Anaphes victus Huber (Hymenoptera: Mymaridae) by examining two special cases of intraspecific discrimination: the recognition of different biotypes (i.e. genotypic discrimination) and the recognition of close relatives (i.e. kin discrimination). Female A. victus had to choose between two categories of parasitized eggs in petri dishes. They were able to discriminate between biotypes and always preferred to oviposit in eggs parasitized by females of other biotypes rather than by females of their own biotype. Females were also able to discriminate between their sisters and unrelated conspecifics and preferred to oviposit in eggs parasitized by unrelated females, but did not discriminate between their sisters and themselves. These results suggest that there is a polymorphic genetic component in host discrimination and that such a preference could induce a reduction in gene flow between populations. That this discrimination system shares many analogies with the complex system of communication of social Hymenoptera is discussed.     

PIP2 signaling in lipid domains: a critical re-evaluation

Microdomains such as rafts are considered as scaffolds for phosphatidylinositol (4,5) bisphosphate (PIP2) signaling, enabling PIP2 to selectively regulate different processes in the cell. Enrichment of PIP2 in microdomains was based on cholesterol-depletion and detergent-extraction studies. Here we show that two distinct phospholipase C-coupled receptors (those for neurokinin A and endothelin) share the same, homogeneously distributed PIP2 pool at the plasma membrane, even though the neurokinin A receptor is localized to microdomains and is cholesterol dependent in its PIP2 signaling whereas the endothelin receptor is not. Our experiments further indicate that detergent treatment causes PIP2 clustering and that cholesterol depletion interferes with basal, ligand-independent recycling of the neurokinin A receptor, thereby providing alternative explanations for the enrichment of PIP2 in detergent-insoluble membrane fractions and for the cholesterol dependency of PIP2 breakdown, respectively.     

The amniotic fluid: an important priming role in kin recognition

The ability of individuals to learn prenatally about their amniotic fluid may be of particular importance in the development of kin recognition, ensuring that individuals learn about genetically related conspecifics. Rat pups, 8 h old, were tested for their preference between their mother's amniotic fluid and that from an unrelated rat. The pups preferred their mother's fluid. Furthermore, pups born by Caesarean section, when tested immediately after birth, preferred their mother's fluid to that of an unrelated rat, indicating that this preference is acquired prenatally. Thus, at birth, rats may possess a rudimentary idea of who their kin are, and prefer and orient towards them, ensuring that any further learning of kinship information is from genetically related conspecifics.     

The evolution of the terrestrial vertebrates: environmental and physiological considerations

Physiological evidence has long been used to suggest that the gnathostomous vertebrates (those possessing jaws) were primitively fresh water. The same was also the case for the Osteichthyes (bony fish) and the Tetrapoda (Amphibia, Reptilia, Aves, Mammalia). However, the geological evidence favours a marine origin for the vertebrates as a whole, and, for the gnathostomes and the osteichthyans in particular. Some of the earliest amphibian remains may be associated with tidally influenced sediments. Furthermore, during the early part of the Devonian, fresh water chemistry may well have been different from that of today, lessening the divide between marine and non-marine environments. Urea formation via the ornithine cycle, and urea retention in the body fluids, are useful adaptations for terrestrial life. They prevent excessive water loss associated with the elimination of nitrogenous waste. These abilities may have been primitive for the gnathostomes, and were developed in the marine environment to reduce osmotic dehydration. In the aqueous medium, gaseous exchange is effected by the gills. These organs are, on the whole, useless in air. For vertebrates, air-breathing is effected by an inflatable sac, with moist linings, and an internal location. Some form of air-breathing sac was primitive for the osteichthyans, and may have been primitive for the gnathostomes. Again, this adaptation for terrestrial life developed in response to conditions experienced in the marine, aquatic environment. A new model of tetrapod evolution is proposed in the light of the basic marine origin and character of the ancestors of the tetrapods.     

The evolution of trans-generational altruism: kin selection meets niche construction

A cornerstone result of sociobiology states that limited dispersal can induce kin competition to offset the kin selected benefits of altruism. Several mechanisms have been proposed to circumvent this dilemma but all assume that actors and recipients of altruism interact during the same time period. Here, this assumption is relaxed and a model is developed where individuals express an altruistic act, which results in posthumously helping relatives living in the future. The analysis of this model suggests that kin selected benefits can then feedback on the evolution of the trait in a way that promotes altruistic helping at high rates under limited dispersal. The decoupling of kin competition and kin selected benefits results from the fact that by helping relatives living in the future, an actor is helping individuals that are not in direct competition with itself. A direct consequence is that behaviours which actors gain by reducing the common good of present and future generations can be opposed by kin selection. The present model integrates niche-constructing traits with kin selection theory and delineates demographic and ecological conditions under which altruism can be selected for; and conditions where the 'tragedy of the commons' can be reduced.