On the evolutionary implications of being a social animal
Does sociality affect evolutionary speed?
Recommendation: posted 27 November 2023, validated 29 November 2023
Greenfield, M. (2023) On the evolutionary implications of being a social animal. Peer Community in Evolutionary Biology, 100652. 10.24072/pci.evolbiol.100652
What does it mean to be highly social? Considering the so-called four ‘pinnacles’ of animal society (Wilson, 1975) – humans, cooperative breeding as found in some non-human mammals and birds, the social insects, and colonial marine invertebrates – having inter-individual relations extending beyond the sexual pair and the parent-offspring interaction is foremost. In many cases being social implies a high local population density, interaction with the same group of individuals over an extended time period, and an overlapping of generations. Additional features of social species may be a wide geographical range, perhaps associated with ecological and behavioral plasticity, the latter often facilitated by cultural transmission of traditions.
Narrowing our perspective to the domain of PCI Evolutionary Biology, we might continue our question by asking whether being social predisposes one to a special evolutionary path toward the future. Do social species evolve faster (or slower) than their more solitary relatives such that over time they are more unlike (or similar to) those relatives (anagenesis)? And are evolutionary changes in social species more or less likely to be accompanied by lineage splitting (cladogenesis) and ultimately speciation? The latter question is parallel to one first posed over 40 years ago (West-Eberhard, 1979; Lande, 1981) for sexually selected traits: Do strong mating preferences and conspicuous courtship signals generate speciation via the Fisherian process or ecological divergence? An extensive survey of birds had found little supporting evidence (Price, 1998), but a recent one that focused on plumage complexity in tanagers did reveal a relationship, albeit a weak one (Price-Waldman et al., 2020). Because sexual selection has been viewed as a part of the broader process of social selection (West-Eberhard, 1979), it is thus fitting to extend our surveys to the evolutionary implications of being social.
Unlike the inquiry for a sexual selection - evolutionary change connection, a social behavior counterpart has remained relatively untreated. Diverse logistical problems might account for this oversight. What objective proxies can be used for social behavior, and for the rate of evolutionary change within a lineage? How many empirical studies have generated data from which appropriate proxies could be extracted? More intractable is the conundrum arising from the connectedness between socially- and sexually-selected traits. For example, the elevated population density found in highly social species can greatly increase the mating advantage enjoyed by an attractive male. If anagenesis is detected, did it result from social behavior or sexual selection? And if social behavior leads to a group structure in which male-male competition is reduced, would a modest rate of evolutionary change be support for the sexual selection - evolutionary speed connection or evidence opposing the sociality - evolution one?
Against the above odds, several biologists have begun to explore the notion that social behavior just might favor evolutionary speed in either anagenesis or cladogenesis. In a recent analysis relying on the comparative method, Lluís Socias-Martínez and Louise Rachel Peckre (2023) combed the scientific literature archives and identified those studies with specific data on the relationships between sexual selection or social behavior and evolutionary change, either anagenesis or cladogenesis. The authors were careful to employ fairly conservative criteria for including studies, and the number eventually retained was small. Nonetheless, some patterns emerge: Many more studies report anagenesis than cladogenesis, and many more report correlations with sexually-selected traits than with non-sexual social behavior ones. And, no study indicates a potential effect of social behavior on cladogenesis. Is this latter observation authentic or an artifact of a paucity of data? There are some a priori reasons why cladogenesis may seldom arise. Whereas highly social behavior could lead to fission encompassing mutually isolated population clusters within a species, social behavior may also engender counterbalancing plasticity that allows and even promotes inter-cluster migration and fusion. And briefly – and non-systematically, as the rate of lineage splitting would need to be measured – looking at one of the pinnacles of animal social behavior, the social insects, there is little indication that diversification has been accelerated. There are fewer than 3000 described species of termites, only ca. 16,000 ants, and the vast majority of bees and wasps are solitary.
Lluís Socias-Martínez and Louise Rachel Peckre provide us with a very detailed discussion of these and a myriad of other complications. I end with a common refrain, we need more consideration of the authors’ interesting question, and much more data and analysis. One can thank Socias-Martínez and Peckre for pointing us in that direction.
Lande, R. (1981). Models of speciation by sexual selection on polygenic traits. Proc. Natn. Acad. Sci. USA 78, 3721-3725. https://doi.org/10.1073/pnas.78.6.3721
Price, T. (1998). Sexual selection and natural selection in bird speciation. Phil. Trans. Roy. Soc. B, 353, 251-260. https://doi.org/10.1098/rstb.1998.0207
Price‐Waldman, R. M., Shultz, A. J., & Burns, K. J. (2020). Speciation rates are correlated with changes in plumage color complexity in the largest family of songbirds. Evolution, 74(6), 1155–1169. https://doi.org/10.1111/evo.13982
Socias-Martínez and Peckre. (2023). Does sociality affect evolutionary speed? Zenodo, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.5281/zenodo.10086186
West-Eberhard, M. J. (1979). Sexual selection, social competition, and evolution. Proceedings of the American Philosophical Society, 123(4), 222–234. http://www.jstor.org/stable/2828804
Wilson, E. O. (1975). Sociobiology. The New Synthesis. Cambridge, Mass., The Belknap Press of Harvard University
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article. The authors declared that they comply with the PCI rule of having no financial conflicts of interest in relation to the content of the article.
"The authors declare that they have received no specific funding for this study"
Evaluation round #2
DOI or URL of the preprint: https://doi.org/10.5281/zenodo.8397348
Version of the preprint: 2
Author's Reply, 08 Nov 2023
Decision by Michael D Greenfield, posted 07 Oct 2023, validated 09 Oct 2023
The revised version of 'Does sociality affect evolutionary speed?' is markedly improved, having addressed many of the issues raised in the review of the initial version. However, several problems remain and need to be corrected before I can recommend the preprint.
Figure 3 is an excellent summary of the results, but some details seem to be missing from its description. In particular, effect magnitude for a positive influence can be 1 or 0.5, but it is not clear how these different magnitudes were assessed using information from the original studies, which used different methods, sample sizes, etc. Similarly, more information on the key words, notably the connectors (i.e. and, or, not, etc) applied between key words, used in identifying relevant studies from the literature should be provided. This precision would be standard in any meta-analysis.
English language : Overall, the English is quite good, but there are still a great many errors : Lack of agreement between subject and verb, inappropriate words used, unusual spelling, etc. In some cases these errors will pose problems for readers whose first language is not English, and they need to be corrected. Please have the entire text checked competently.
Discussion. While the text from the beginning to line 498 is generally clear and of appropriate length, the discussion that follows is excessively long, and many parts are far too complicated as written. I advise a discussion that is reduced by at least 50%, that covers the main problems encountered in studying the sociality - evolutionary speed question in a concise and straightforward manner, and avoids lengthy attention to individual studies. The current version of the discussion, with many convoluted arguments and run-on sentences, is likely to lose the attention of readers rather quickly. In your revision focus on cogent presentations that do not require boldface highlighting of terms in the text, a feature that is generally not found in the published literature.
Evaluation round #1
DOI or URL of the preprint: https://doi.org/10.5281/zenodo.7693687
Version of the preprint: 1
Author's Reply, 02 Oct 2023
Decision by Michael D Greenfield, posted 27 May 2023, validated 30 May 2023
It is clear from the reviews by the two referees, and from my own reading, that this manuscript concerns a novel and important topic in evolutionary biology and should eventually be published pending careful revisions. Both referees were enthusiastic about the topic but also pointed out several major problems that need to be addressed. I agree with their points and emphasize the following : 1) More attention should be paid to the objectivity of 'proxies' for evolution and (particularly) for sociality. 2) Focus on the nuances of the selectionist and population approaches to the issue. 3) It is not surprising that a uniform conclusion is not reached (sociality appears to be correlated with higher evolution rates ; or, alternatively, with lower rates or is uncorrelated), but can you infer the situations where such correlation holds and where it does not? 4) The overall presentation should be more cogent, with attention paid to organization of the manuscript and general writing style.