Evolution: Kin selection spreads
Charles Darwin considered the evolution of altruism to be a puzzle (Darwin, 1871). Altruistic acts benefit the recipient but may cost the actor, making it difficult to grasp how they could have evolved in a world where organisms compete to survive. Since individuals who act selfishly should fare better than those with altruistic tendencies, shouldn’t altruism be quickly selected against?
An elegant solution to this problem emerged in the 1930s, when mathematical arguments were laid out to show how genes that enable altruistic behaviors could spread through a population (Fisher, 1930; Haldane, 1932). These ideas were further developed in the 1960s by W.D. ‘Bill’ Hamilton, and later re-derived by George Price (Hamilton, 1964a; Hamilton, 1964b; Price, 1972).
This work showed that if the individual(s) receiving altruistic acts are genetically related to the altruistic actor, and if an altruistic act is sufficiently beneficial to the receivers relative to the costs to the actor, then altruistic behaviors can spread. This process was named ‘kin selection’ (Smith, 1964). A swathe of additional terms were then coined, including ‘indirect fitness’ (the benefits associated with promoting the offspring of relatives) and ‘inclusive fitness’ (the sum total of direct and indirect fitness). These theoretical developments set the stage for thousands of empirical studies of social behavior. Now, in eLife, Marie Charpentier and colleagues in France, Germany and Gabon – including joint first author Clémence Poirotte – report intriguing new evidence which deepens our understanding of how kin selection may take place within complex societies (Charpentier et al., 2022).
The study took place in a free-ranging population of mandrills living in Gabon. These large and colorful ground-dwelling monkeys live in societies structured around groups of closely related females who share a maternal ancestor, with mature males joining the group during the mating season to sire offspring. As for other social mammals, the health and success of an individual is often shaped by their family connections and how well they are integrated in to the community.
Building on their previous work, Charpentier et al. used machine learning to train a human face recognition algorithm on a large database of mandrill face pictures. The program was then used on the study population to show that infants with the same father look alike – more so than unrelated individuals or maternal half-siblings. Long-term behavioral observations then revealed that mothers spend more time close to infants whose faces resemble their own offspring’s. Such patterns may result in paternal half-siblings interacting with each other more frequently, and potentially may lead to the establishment of social relationships between paternally related infants. Lastly, Charpentier et al. build a theoretical model which demonstrates that mothers would gain fitness benefits by promoting altruistic acts among offspring sired by the same father.
Several factors could explain how increased associations may emerge between siblings who share a father. For example, these related infants may have more similar nutritional needs or digestive processes, and hence find themselves in the same feeding areas more often. Charpentier et al. address one such alternative hypothesis: that fathers may be driving these interactions, for example by spending more time with the mothers they have mated with, or with the babies they have sired. They show that this mechanism is unlikely to explain their results, in part because paternal care is thought to be rare or absent, and because many males are not present within the group outside of the mating season.
As the movement of mandrill infants is primarily determined by their mother, Charpentier et al. reason that it is most likely to be maternal behavior that drives interactions between similar-looking infants. While classic kin selection posits that a mother might increase her fitness by interacting with genetically related individuals, the team argues that female mandrills may ensure that their offspring has better survival outcomes by fostering relationships with non-kin individuals (their infant’s paternal half siblings). They term this process ‘second-order kin selection’.
The work by Charpentier et al. features a particularly rich and diverse set of methods, combining digital images, genetics, machine learning, long-term behavioral observations, and theoretical modeling. Together, these approaches result in an impressive analysis and argument which provoke new questions on how indirect fitness effects might manifest, and the kinds of social behaviors that might be explained by kin selection. Overall, this study adds an intriguing new layer to the mechanisms by which kin selection might operate, and to our understanding of the complexity of evolved social behaviors.
References
-
BookThe Descent of Man, and Selection in Relation to SexNew York: John Murray.https://doi.org/10.5962/bhl.title.24784
-
BookThe genetical theory of natural selectionClarendon Press.https://doi.org/10.5962/bhl.title.27468
-
Fisher’s “fundamental theorem” made clearAnnals of Human Genetics 36:129–140.https://doi.org/10.1111/j.1469-1809.1972.tb00764.x
Article and author information
Author details
Publication history
- Version of Record published: November 24, 2022 (version 1)
Copyright
© 2022, Higham
This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 387
- Page views
-
- 37
- Downloads
-
- 0
- Citations
Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Ecology
- Genetics and Genomics
Adulis, located on the Red Sea coast in present-day Eritrea, was a bustling trading centre between the first and seventh centuries CE. Several classical geographers--Agatharchides of Cnidus, Pliny the Elder, Strabo-noted the value of Adulis to Greco--Roman Egypt, particularly as an emporium for living animals, including baboons (Papio spp.). Though fragmentary, these accounts predict the Adulite origins of mummified baboons in Ptolemaic catacombs, while inviting questions on the geoprovenance of older (Late Period) baboons recovered from Gabbanat el-Qurud ('Valley of the Monkeys'), Egypt. Dated to ca. 800-540 BCE, these animals could extend the antiquity of Egyptian-Adulite trade by as much as five centuries. Previously, Dominy et al. (2020) used stable istope analysis to show that two New Kingdom specimens of P. hamadryas originate from the Horn of Africa. Here, we report the complete mitochondrial genomes from a mummified baboon from Gabbanat el-Qurud and 14 museum specimens with known provenance together with published georeferenced mitochondrial sequence data. Phylogenetic assignment connects the mummified baboon to modern populations of Papio hamadryas in Eritrea, Ethiopia, and eastern Sudan. This result, assuming geographical stability of phylogenetic clades, corroborates Greco-Roman historiographies by pointing toward present-day Eritrea, and by extension Adulis, as a source of baboons for Late Period Egyptians. It also establishes geographic continuity with baboons from the fabled Land of Punt (Dominy et al., 2020), giving weight to speculation that Punt and Adulis were essentially the same trading centres separated by a thousand years of history.
-
- Ecology
While bacterial diversity is beneficial for the functioning of rhizosphere microbiomes, multi-species bioinoculants often fail to promote plant growth. One potential reason for this is that competition between different species of inoculated consortia members creates conflicts for their survival and functioning. To circumvent this, we used transposon insertion mutagenesis to increase the functional diversity within Bacillus amyloliquefaciens bacterial species and tested if we could improve plant growth promotion by assembling consortia of highly clonal but phenotypically dissimilar mutants. While most insertion mutations were harmful, some significantly improved B. amyloliquefaciens plant growth promotion traits relative to the wild-type strain. Eight phenotypically distinct mutants were selected to test if their functioning could be improved by applying them as multifunctional consortia. We found that B. amyloliquefaciens consortium richness correlated positively with plant root colonization and protection from Ralstonia solanacearum phytopathogenic bacterium. Crucially, 8-mutant consortium consisting of phenotypically dissimilar mutants performed better than randomly assembled 8-mutant consortia, suggesting that improvements were likely driven by consortia multifunctionality instead of consortia richness. Together, our results suggest that increasing intra-species phenotypic diversity could be an effective way to improve probiotic consortium functioning and plant growth promotion in agricultural systems.