Of the various forms of cooperative and altruistic behavior, reciprocity remains the most contentious. Humans certainly exhibit reciprocity – under certain circumstances – and various non-human animals behave in ways suggesting that they do as well. Thus, evolutionary biologists have sought to explain why non-relatives might engage in altruistic transactions when a substantial delay occurs between helping and compensation; i.e. an individual may be a donor today and a beneficiary tomorrow, or vice-versa. This quest, aided by game theory and computer modeling late in the past century, identified some strategies for reciprocal behavior that could work – in theory. But when biologists looked for confirmation of these strategies in animals they found little evidence that stood up to rigorous testing. In a recent paper André and Nolfi [1] offer a compelling reason for this observed rarity of reciprocity: Reciprocal behavior that animals might exhibit is a bit more complex than any of the game theoretic strategies, and even the simplest forms of realistic behavior would entail several nearly simultaneous mutations, an unlikely occurrence. André and Nolfi [1] relied on neural networks to test actors, robots that could evolve helping and reciprocal behavior from a basal level of selfishness. In an extensive series of simulations, they found that reciprocal behavior did not take hold in a population, largely because the various intermediates to full reciprocity were eliminated before the subsequent mutations occurred. The findings are satisfying given our current knowledge of animal behavior, but questions remain. Notably, how does one account for those rare cases in which reciprocity does meet all the criteria? The authors suggest some possibilities, but an analysis will await their next study.

Reference

[1] André J-B, Nolfi S. 2016. Evolutionary robotics simulations help explain why reciprocity is rare in nature. Scientific Reports 6:32785. doi: 10.1038/srep32785

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.

References

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

Historically neglected or considered a rare aberration in animals under the biological species concept, interspecific hybridisation has by now been recognised to be taxonomically widespread, particularly in rapidly diversifying groups (Dagilis et al. 2021; Edelman & Mallet 2021; Mallet et al. 2016; Seehausen 2004). Yet the prevalence of introgressive hybridizations, its evolutionary significance, and its impact on species diversification remain a hot topic of research in evolutionary biology. The rapid increase in genomic resources now available for non-model species has significantly contributed to the detection of introgressive hybridization across taxa showing that reticulated evolution is far more common in the animal kingdom than historically considered. Yet, detecting it, quantifying its magnitude, and assessing its evolutionary significance remains a challenging endeavour with constantly evolving methodologies to better explore and exploit genomic data (Blair & Ané 2020; Degnan & Rosenberg 2009; Edelman & Mallet 2021; Hibbins & Hahn 2022).

In the marine realm, the dearth of geographic barriers and the large dispersal abilities of pelagic species like cetaceans have raised the questions of how populations and species can diverge and adapt to distinct ecological conditions in face of potentially large gene-flow, the so-called marine speciation paradox (Bierne et al. 2003). Contemporaneous hybridization among cetacean species has been widely documented in nature despite large phenotypic differences (Crossman et al. 2016). The historical prevalence of reticulated evolution, its evolutionary significance, and how it might have impacted the evolutionary history and diversification of the cetaceans have however remained elusive so far. Recent phylogenomic studies suggested that introgression has been prevalent in cetacean evolutionary history with instances reported among baleen whales (mysticetes) (Árnason et al. 2018) and among toothed whales (odontocetes), especially in the rapidly diversifying dolphins family of the Delphininae (Guo et al. 2021; Moura et al. 2020).

Analysing publicly available whole-genome data from nine cetacean species across three families of Delphinoidae – dolphins, porpoises, and monondontidae – using phylogenomics and demo-genetics approaches, Westbury and colleagues (2022) take a step further in documenting that evolution among these species has been far from a simple bifurcating tree. Instead, their study describes widespread occurrences of introgression among Delphinoidae, drawing a complex picture of reticulated evolutionary history. After describing major topology discordance in phylogenetic gene trees along the genome, the authors use a panel of approaches to disentangle introgression from incomplete lineage sorting (ILS), the two most common causes of tree topology discordances (Hibbins & Hahn 2022). Applying popular tests that separate introgression from ILS, such as the Patterson’s D (a.k.a. ABBA-BABA) test (Durand et al. 2011; Green et al. 2010), QuIBL (Edelman et al. 2019), and D-FOIL (Pease & Hahn 2015), the authors report that signals of introgression are present in the genomes of most (if not all) the cetacean species included in their study. However, this picture needs to be nuanced. Most introgression signals seem to echo old introgression events that occurred primarily among ancestors. This is suggested by the differential signals of topology discordance along the genome when considering sliding windows along the genome of varying sizes (50kb, 100kb, and 1Mb), and by patterns of excess derived allele sharing along branches of the species tree, as captured by the f-branch test (Malinsky et al. 2021; Malinsky et al. 2018). The authors further investigated the dynamic of cessation of gene flow (and/or ILS) between species using the F1 hybrid PSMC (or hPSMC) approach (Cahill et al. 2016). By estimating the cross-coalescent rates (CRR) between species pairs with time in light of previously estimated species divergence times (McGowen et al. 2020), the authors report that gene flow (and/or ILS) most likely has stopped by now among most species, but it may have lasted for more than half of the time since the species split from each other. According to the author, this result may reflect the slow process by which reproductive isolation would have evolved between cetacean lineages, and that species isolation was marked by significant introgression events.

Now, while the present study provides a good overview of how complex is the reticulated evolutionary history of the Delphinoidae, getting a complete picture will require overcoming a few important limitations. The first ones are methodological and related to the phylogenomic analyses. Given the sampling design with one diploid genome per species, the authors could not phase the data into the parental haplotypes, but instead relied on a majority consensus creating mosaic haploidized genomes representing a mixture between the two parental copies. Moreover, by using large genomic windows (≥50kb) that likely span multiple independent loci, phylogenetic analyses in windows encompassed distinct phylogenetic signals, potentially leading to bias and inaccuracy in the inferences. Thawornwattana et al (2018) previously showed that this “concatenation approach”  could significantly impact phylogenetic inferences. They proposed instead to use loci small enough to minimise the risk of intra-locus recombination and to consider them in blocks of non-recombining loci along the genome in order to conduct phylogenetic analysed, ideally under the multi-species coalescent (MSC) that can account for ILS (e.g. BPP; Flouri et al. 2018; Jiao et al. 2020; Yang 2015). Such an approach applied to the diversification of the Delphinidae may reveal substantial changes compared to the currently admitted species tree.

Inaccuracy in the species tree estimation may have a major impact on the introgression analyses conducted in this study since the species tree and branching order must be supplied in the introgression analyses to properly disentangle introgression from ILS. Here, the authors rely on the tree topology that was previously estimated in McGowen et al. (2020), which they also recovered using their consensus estimation from ASTRAL-III (Zhang et al. 2018). While the methodologies accounted to a certain extent for ILS, albeit with potential bias induced by the concatenation approach, they ignore the presumably large amount of introgression among species during the diversification process. Estimating species branching order while ignoring introgression can lead to major bias in the phylogenetic inference and can lead to incorrect topologies. Even if these MSC-based methods account for ILS, inferences can become very inaccurate or even break down as gene flow increases (see for ex. Jiao et al. 2020; Müller et al. in press; Solís-Lemus et al. 2016). Dedicated approaches have been developed to model explicitly introgression together with ILS to estimate phylogenetic networks (Blair & Ané 2020; Rabier et al. 2021) or in isolation-with-migration model (Müller et al. in press; Wang et al. 2020). Future studies revisiting the reticulated evolutionary history of the Delphinoidae with such approaches may not only precise the species branching order, but also deliver a finer view of the magnitude and prevalence of introgression during the evolutionary history of these species.

A final part of Westbury et al. (2022)'s study set out to test whether historical periods of low abundance could have facilitated hybridization among Delphinoidae species. During these periods of low abundance, species may encounter only a limited number of conspecifics and may consider individuals from other species as suitable mating partners, leading to hybridisation (Crossman et al. 2016; Edwards et al. 2011; Westbury et al. 2019). The authors tested this hypothesis by considering genome-wide genetic diversity (or heterozygosity) as a proxy of historical effective population size (Ne), itself as a proxy of the evolution of census size with time. They also try to link historical Ne variation (from PSMC, Li & Durbin 2011) with their estimated time to cessation of gene flow or ILS (from the CRR of hPSMC). However, no straightforward relationship was found between the genetic diversity and the propensity of species to hybridize, nor was there any clear link between Ne variation through time and the cessation of gene flow or ILS. Such a lack of relationship may not come as a surprise, since the determinants of genome-wide genetic diversity and its variation through evolutionary time-scale are far more diverse and complex than just a direct link with hybridization, introgression, or even with the census population size. In fact, genetic diversity results from the balance between all the evolutionary processes at play in the species' evolutionary history (see the review of Ellegren & Galtier 2016). Other important factors can strongly impact genetic diversity, including demography and structure, but also linked selection (Boitard et al. 2022; Buffalo 2021; Ellegren & Galtier 2016). 

All in all, Westbury and coll. (2022) present here an interesting study providing an additional step towards resolving and understanding the complex evolutionary history of the Delphinoidae, and shedding light on the importance of introgression during the diversification of these cetacean species. Prospective work improving upon the taxonomic sampling, with additional genomic data for each species, considered with dedicated approaches tailored at estimating species tree or network while accounting for ILS and introgression will be key for refining the picture depicted in this study. Down the road, altogether these studies will contribute to assessing the evolutionary significance of introgression on the diversification of Delphinoides, and more generally on the diversification of cetacean species, which still remain an open and exciting perspective. 

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Studying the effects of speciation, hybridisation, and evolutionary outcomes following reproduction from divergent populations is a major research area in evolutionary genetics [1]. There are two phenomena that have been the focus of contemporary research. First, a classic concept is the formation of ‘Bateson-Dobzhansky-Muller’ incompatibilities (BDMi) [2–4] that negatively affect hybrid fitness. Here, two diverging populations accumulate mutations over time that are unique to that subpopulation. If they subsequently meet, then these mutations might negatively interact, leading to a loss in fitness or even a complete lack of reproduction. BDMi formation can be complex, involving multiple genes and the fitness changes can depend on the direction of introgression [5]. Second, such secondary contact can instead lead to heterosis, where offspring are fitter than their parental progenitors [6].

Understanding which outcomes are likely to arise require one to know the potential fitness effects of mutations underlying reproductive isolation, to determine whether they are likely to reduce or enhance fitness when hybrids are formed. This is far from an easy task, as it requires one to track mutations at several loci, along with their effects, across a fitness landscape.

The work of De Sanctis et al. [7] neatly fills in this knowledge gap, by creating a general mathematical framework for describing the consequences of a cross from two divergent populations. The derivations are based on Fisher’s Geometric Model, which is widely used to quantify selection acting on a general fitness landscape that is affected by several biological traits [8,9], and has previously been used in theoretical studies of hybridisation [10–12]. By doing so, they are able to decompose how divergence at multiple loci affects offspring fitness through both additive and dominance effects.

A key result arising from their analyses is demonstrating how offspring fitness can be captured by two main functions. The first one is the ‘net effect of evolutionary change’ that, broadly defined, measures how phenotypically divergent two populations are. The second is the ‘total amount of evolutionary change’, which reflects how many mutations contribute to divergence and the effect sizes captured by each of them. The authors illustrate these measurements using simulations covering different scenarios, demonstrating how different parental states can lead to similar fitness outcomes. They also propose experimental methods to measure the underlying mutational effects.

This study neatly demonstrates how complex genetic phenomena underlying hybridisation can be captured using fairly simple mathematical formulae. This powerful approach will thus open the door for future research to investigate hybridisation in more detail, whether it is by expanding on these theoretical models or using the elegant outcomes to quantify fitness effects in experiments.

 

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In this study, Ishigohoka and colleagues tackle an important, yet often overlooked, question on the causes of genetic variation. While genome-wide patterns represent population structure, local variation is often associated with selection. Authors propose that an alternative cause for variation in individual loci is reduced recombination rate.

To test this hypothesis, authors perform local Principal Component Analysis (PCA) (Li & Ralph, 2019) to identify local deviations in population structure in the Eurasian blackcap (Sylvia atricapilla) (Ishigohoka et al. 2022). This approach is typically used to detect chromosomal rearrangements or any long region of linked loci (e.g., due to reduced recombination or selection) (Mérot et al. 2021). While other studies investigated the effect of low recombination on genetic variation (Booker et al. 2020), here authors provide a comprehensive analysis of the effect of recombination to local PCA patterns both in empirical and simulated data sets. Findings demonstrate that low recombination (and not selection) can be the sole explanatory variable for outlier windows. The study also describes patterns of genetic variation along the genome of Eurasian blackcaps, localising at least two polymorphic inversions (Ishigohoka et al. 2022).

Further investigations on the effect of model parameters (e.g., window sizes and thresholds for defining low-recombining regions), as well as the use of powerful neutrality tests are in need to clearly assess whether outlier regions experience selection and reduced recombination, and to what extent.

References

Booker, T. R., Yeaman, S., & Whitlock, M. C. (2020). Variation in recombination rate affects detection of outliers in genome scans under neutrality. Molecular Ecology, 29 (22), 4274–4279. https://doi.org/10.1111/mec.15501

Ishigohoka, J., Bascón-Cardozo, K., Bours, A., Fuß, J., Rhie, A., Mountcastle, J., Haase, B., Chow, W., Collins, J., Howe, K., Uliano-Silva, M., Fedrigo, O., Jarvis, E. D., Pérez-Tris, J., Illera, J. C., Liedvogel, M. (2022) Distinct patterns of genetic variation at low-recombining genomic regions represent haplotype structure. bioRxiv 2021.12.22.473882, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2021.12.22.473882

Li, H., & Ralph, P. (2019). Local PCA Shows How the Effect of Population Structure Differs Along the Genome. Genetics, 211 (1), 289–304. https://doi.org/10.1534/genetics.118.301747

Mérot, C., Berdan, E. L., Cayuela, H., Djambazian, H., Ferchaud, A.-L., Laporte, M., Normandeau, E., Ragoussis, J., Wellenreuther, M., & Bernatchez, L. (2021). Locally Adaptive Inversions Modulate Genetic Variation at Different Geographic Scales in a Seaweed Fly. Molecular Biology and Evolution, 38 (9), 3953–3971. https://doi.org/10.1093/molbev/msab143