Mountain gorillas maintain strong affiliative biases for maternal siblings despite high male reproductive skew and extensive exposure to paternal kin

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    Evaluation Summary:

    This study investigates the potential role of kin selection in driving social behaviours among siblings in wild mountain gorillas. Using an impressive dataset of 14 years for 157 individuals the authors find some evidence for kin recognition in guiding biases for affiliative and aggressive behaviours. However, the results of the current study will be more convincing if a number of major concerns with the analysis can be addressed.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)

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Evolutionary theories predict that sibling relationships will reflect a complex balance of cooperative and competitive dynamics. In most mammals, dispersal and death patterns mean that sibling relationships occur in a relatively narrow window during development and/or only with same-sex individuals. Besides humans, one notable exception is mountain gorillas, in which non-sex-biased dispersal, relatively stable group composition, and the long reproductive tenures of alpha males mean that animals routinely reside with both maternally and paternally related siblings, of the same and opposite sex, throughout their lives. Using nearly 40,000 hr of behavioral data collected over 14 years on 699 sibling and 1235 non-sibling pairs of wild mountain gorillas, we demonstrate that individuals have strong affiliative preferences for full and maternal siblings over paternal siblings or unrelated animals, consistent with an inability to discriminate paternal kin. Intriguingly, however, aggression data imply the opposite. Aggression rates were statistically indistinguishable among all types of dyads except one: in mixed-sex dyads, non-siblings engaged in substantially more aggression than siblings of any type. This pattern suggests mountain gorillas may be capable of distinguishing paternal kin but nonetheless choose not to affiliate with them over non-kin. We observe a preference for maternal kin in a species with a high reproductive skew (i.e. high relatedness certainty), even though low reproductive skew (i.e. low relatedness certainty) is believed to underlie such biases in other non-human primates. Our results call into question reasons for strong maternal kin biases when paternal kin are identifiable, familiar, and similarly likely to be long-term groupmates, and they may also suggest behavioral mismatches at play during a transitional period in mountain gorilla society.

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  1. Evaluation Summary:

    This study investigates the potential role of kin selection in driving social behaviours among siblings in wild mountain gorillas. Using an impressive dataset of 14 years for 157 individuals the authors find some evidence for kin recognition in guiding biases for affiliative and aggressive behaviours. However, the results of the current study will be more convincing if a number of major concerns with the analysis can be addressed.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)

  2. Reviewer #1 (Public Review):

    This manuscript sets up a well-reasoned study and capitalizes on a very impressive long-term dataset. Their methods are generally sound and well explained. The argument for paternal kin recognition here could be compelling, but at this stage, it does not seem possible to rule out a simpler cognitive mechanism, i.e. gorillas direct their aggression toward unfamiliar and/or outgroup individuals. The authors note the difficulty of indexing familiarity versus kinship because there were very few out-group dyads (two individuals from different natal groups) that were related. But were there any in-group dyads that were not related? If so, then it might be plausible to add the natal group as a co-variate to parse these mechanisms. A result in either direction could be very compelling. Another concern is dealing with age- which is incredibly difficult with data like this and the authors have offered a reasonable compromise here by settling on a single term (age difference). It makes good sense that the difference in age between two partners should contribute to shaping the interactions between a dyad, however, each of the social behaviors here is more or less common depending on age in most species (including gorillas to the best of my knowledge) with social play generally decreasing with age while social grooming and aggression increase. I understand that it is not the intent of this manuscript to describe the ontogeny of social bonds, however, as the dataset includes individuals ranging from infants through adults, is it possible that such age-related changes in social behavior are affecting the results? Whether or not the authors find strong indications that gorillas can recognize paternal kin, specifically, beyond in-group/out-group familiarity, this manuscript represents an important contribution to the field.

  3. Reviewer #2 (Public Review):

    Unlike most species, mountain gorillas may spend most of their lives around siblings of either sex, as well as among unrelated individuals. This offers an opportunity to test how maternal and paternal relatedness and sex affect cooperation and competition, which the authors capitalized on using an impressive 40'000 hours of behavioral observations. The results show a clear preference for full siblings and maternal half-siblings in affiliative behaviors (play and grooming), with play being most common among male-male dyads, grooming among female-female dyads, and both play and grooming declining with increasing age difference. In contrast, aggression was most common among unrelated individuals, especially among male-female dyads, and equally low among full sibs, maternal half-sibs, and paternal half-sibs. Given the large sample size and adequate statistical methods, these results appear credible and robust.

    The authors interpret these findings to imply paternal (and maternal) kin recognition, given the lower rates of aggression, despite a lack of preferential affiliation with paternal kin. To put this into perspective, it's useful to understand that male-female aggression often occurs in the context of mating, so the low rates of aggression among paternal sibs suggest inbreeding avoidance. In contrast, it's less clear what the benefits of affiliation are. Male-male play involves rough-and-tumble that helps develop strength and skills useful in adult contests; maybe maternal kin make for more trustworthy sparring partners. Grooming serves important hygienic functions in primates and is often reciprocated, but it's less clear here whether grooming is also used to cement cooperative bonds useful in other contexts (what do female gorillas compete over/cooperate for, if anything?). Thus, the authors conclude that kin selection does not explain affiliative biases, because paternal sibs are not treated the same as paternal sibs and full sibs; I think this conclusion is slightly too strong given that there were no clear predictions about patterns of affiliation beyond 'higher r = more affiliation'.

    How do gorillas recognize kin? The authors tested the concept of 'familiarity', whereby individuals use exposure to others as a proxy for kinship. They operationalize familiarity by age difference, which I think works well as a cue of paternal kinship (given historically high reproductive skew among gorillas, meaning similarly-aged individuals were likely sired by the same alpha male, but this likelihood decreases as a function of tenure length), though I think it falls short of adequately capturing likely cues of maternal kinship: First, by definition, maternal siblings are of different ages (by at least the length of one interbirth interval, and more than that on average for specific sex combinations). Second, cues of maternal kinship are much more specific than living in the same group and being of a similar age - it minimally involves being around specific other individuals when you are with your mother (i.e. your exposure to others is mediated by your mother), and may include more direct cues like sharing a night nest with your mother and another individual, seeing your mother nurse another individual, etc. The authors try to account for this by adjusting for the mother's presence during interaction periods, but I don't think this fully accounts for the ways mothers structure one's social network, increasing exposure among maternal sibs throughout one's lifetime. Thus, I am also a bit reluctant to accept the second statement in the title, that familiarity doesn't explain affiliative biases, as I don't think the operationalization of familiarity as age difference does justice to the most likely cues of maternal kinship.

  4. Reviewer #3 (Public Review):

    In this study the authors investigated whether mountain gorillas of varying ages behave differently toward their siblings compared to non-siblings, and, how this bias varied based on whether individuals were full or maternal half-siblings vs. paternal siblings, opposite or same-sex siblings, and close or far apart in age (with age as a continuous variable).

    This study has two major strengths:
    One is its long-term dataset. Authors document social interactions for 157 individuals over 14 years on wild mountain gorillas. This is amazing!

    A second major strength is the opportunity this dataset and study system provides to test predictions about proposed mechanisms for kin recognition in primates. The authors do a good job of making these details about their study system and their predictions clear:

    Kin selection is a proposed mechanism for the evolution of cooperative behavior. For it to operate, animals must have some mechanism by which to recognize their genetic kin and affiliate and cooperate differentially with these kin than with non-kin. However primatological studies have revealed that routes to kin recognition that are immediately clear. First, there are many examples of cooperation with non-kin. Second, in certain species, individuals bias affiliation and cooperation toward maternal but not paternal kin. Because these maternal-kin-biased species are ones with low male reproductive skew (many females mate with many males and many males father infants) and where mothers are sole caregivers of offspring, both the mating system and the familiarity of growing up together under the care of the same mother (especially if close in age) are proposed to drive affiliative and cooperative biases. Mountain gorillas provide a strong model to test these predictions because there is low male reproductive skew and individuals may live in cohesive groups with both maternal siblings and paternal siblings of all ages throughout their lives.

    However, this study has two major weaknesses.

    First, it lacks clarity in the actual measures of kin bias: that is - how dyadic social interactions and relationships manifest in mountain gorillas and how these change throughout life as relevant to the measures used.
    For example, the authors provide little information on the ages of the siblings involved in the study (only that the median was 9.7 years). How do these ages match to different developmental stages and dimensions of mountain gorilla social interaction? For instance, the frequency of play, one of the three social affiliative social measures employed, might vary considerably based on age. In many other species, it occurs more often between immature individuals or between a mature and immature individual rather than between mature ones.

    Relatedly, siblings who affiliate frequently do not necessarily need to have reduced aggression. Studies of dyadic affiliative bonds in baboons and chimpanzees both indicate that in certain contexts individuals who affiliate more may also have increased conflict. What might distinguish certain more cooperative bonds from others, for example, is what happens after this conflict. This is not something the authors need to measure in this study but it would be helpful to have such nuances of relationships discussed, or at least to provide the reader with more context for interpreting the behavioral results of affiliation and aggression as assays for kin-bias and potential fitness benefits associated with this bias.

    Second, relatedly - there was no basis provided for the evolutionary function of sibling affiliation - that is, how might affiliation as measured by proximity, grooming, and play, contribute to cooperation and/or improved fitness in mountain gorillas? The existence of some form of dyadic social bond benefit (such as alliances, or improved survival) is necessary for kin selection to be in play. What might the functions of sibling relationships be in mountain gorillas? What are modes of dyadic cooperation like alliances described in other species (e.g. alliances between cercopithecine monkey mothers and sisters)? Providing some theoretical justification/context for the existence of benefits that might be enabled by kin selection in mountain gorillas would strengthen the study considerably.

    One example of where such a nuanced explanation of both social measures and relationship function was provided well is when the authors interpreted their finding that opposite-sex non-siblings showed heightened rates of aggression compared to opposite-sex siblings and same-sex siblings and same-sex non-siblings. Here, they discussed how an opposite-sex non-sibling relationship is one that has functional importance relevant to reproduction and that increased aggression might represent sexual coercion.