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. 2022 Apr 11;32(7):1607-1615.e4.
doi: 10.1016/j.cub.2022.01.082. Epub 2022 Feb 24.

Mechanisms of inbreeding avoidance in a wild primate

Allison A Galezo  1 , Melina A Nolas  2 , Arielle S Fogel  3 , Raphael S Mututua  4 , J Kinyua Warutere  4 , I Long'ida Siodi  4 , Jeanne Altmann  5 , Elizabeth A Archie  6 , Jenny Tung  7 , Susan C Alberts  8
Affiliations

Mechanisms of inbreeding avoidance in a wild primate

Allison A Galezo et al. Curr Biol. .

Abstract

Inbreeding often imposes net fitness costs,1-5 leading to the expectation that animals will engage in inbreeding avoidance when the costs of doing so are not prohibitive.4-9 However, one recent meta-analysis indicates that animals of many species do not avoid mating with kin in experimental settings,6 and another reports that behavioral inbreeding avoidance generally evolves only when kin regularly encounter each other and inbreeding costs are high.9 These results raise questions about the processes that separate kin, how these processes depend on kin class and context, and whether kin classes differ in how effectively they avoid inbreeding via mate choice-in turn, demanding detailed demographic and behavioral data within individual populations. Here, we address these questions in a wild mammal population, the baboons of the Amboseli ecosystem in Kenya. We find that death and dispersal are very effective at separating opposite-sex pairs of close adult kin. Nonetheless, adult kin pairs do sometimes co-reside, and we find strong evidence for inbreeding avoidance via mate choice in kin classes with relatedness ≥0.25. Notably, maternal kin avoid inbreeding more effectively than paternal kin despite having identical coefficients of relatedness, pointing to kin discrimination as a potential constraint on effective inbreeding avoidance. Overall, demographic and behavioral processes ensure that inbred offspring are rare in undisturbed social groups (1% of offspring). However, in an anthropogenically disturbed social group with reduced male dispersal, we find inbreeding rates 10× higher. Our study reinforces the importance of demographic and behavioral contexts for understanding the evolution of inbreeding avoidance.9.

Keywords: baboon; dispersal; inbreeding; inbreeding avoidance; mate choice; primate.

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Conflict of interest statement

Declaration of interests The authors declare no competing interests.

Figures

Figure 1.
Figure 1.. Demographic barriers to adult co-residency in opposite-sex kin whose lifespans overlapped: (A) mother-son pairs, (B) father-daughter pairs, (C) maternal half-siblings, (D) paternal half-siblings.
Each light gray branch of the Sankey diagram represents a reason that an opposite-sex pair did not live together for any length of time as adults. We included all opposite sex pairs with overlapping lifespans and uncensored co-residency length data (i.e. one or both individuals were dead at the time of analysis). “Pre-birth demographic events” include dispersals and group fissions that separate the individuals before the birth of the younger individual. See also Figures S1 and S2.
Figure 2.
Figure 2.. Predicted probabilities, calculated from Bayesian logistic regression models, of a consortship occurring for different categories of female-male pairs, as a function of the male’s dominance rank and controlling for other predictors.
(A) and (B) Results of the main model: Black, gray, and light gray points (± 90% credible intervals) represent the posterior distributions of the probabilities of consortships between different kin classes, involving only fully adult, post-adolescent females in wild-feeding groups. (A) Mother-son pairs and father-daughter pairs had substantially lower probabilities of consorting than unrelated pairs, and mother-son probabilities were lower than father-daughter probabilities. For visualization, the other predictors were set to female rank=1, number of males in the group=10, female age =10 years, and male status=not natal. (B) Maternal half-siblings and paternal half-siblings had substantially lower probabilities of consorting than unrelated pairs, and maternal sibling probabilities were lower than paternal sibling probabilities. Other predictors as in panel A. (C) and (D) Results of the adolescent model: Points and credible intervals represent the posterior distributions of the probabilities of consortship for females experiencing adolescent subfertility (i.e., their first nine sexual cycles after adolescence) versus adult fertility; the analysis was restricted to wild-feeding groups. Other predictors as in panel A. (C) Subfertile adolescent females were more likely to consort with their paternal siblings than adult females were. Note that this pattern is the reverse of the overall effect of adolescent subfertility: subfertile females were in general much less likely to engage in a consortship with any given male (Table 2). (D) Subfertile adolescent females were less likely than adult females to consort with their fathers, consistent with the overall pattern of lower consortship probabilities for subadolescent females. (E) and (F) Results of the Lodge group model: Points and credible intervals represent the posterior distributions of the probabilities of consortship for related versus unrelated female-male pairs in (E) wild-feeding groups and (F) the semi-provisioned Lodge group. All kin categories with r ≥ 0.0625 are collapsed into the ‘related’ category. Other predictors as in panel A. In both wild-feeding groups and the Lodge group, related pairs were less likely to engage in consortships than unrelated pairs. See also Figure S3 and Table S2.
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