A comprehensive study by Roux et al 2024 investigates the impact of eusociality on the efficacy of natural selection in termites, with and additional focus on whether higher levels of social complexity are associated with lower effective population size (Ne) and relaxed purifying selection.

Eusociality is characterized by a division of reproductive labor, cooperative care of offspring, and overlapping generations, and has evolved independently across various animal taxa with the most complex social systems found in Hymenoptera (bees, wasps, ants) and termites. Because reproduction is limited to a few individuals, this leads to a reduced effective population size (Ne), which impacts genome evolution. Smaller Ne increases the influence of genetic drift, weakening the efficiency of natural selection and allowing the accumulation of weakly deleterious mutations. This phenomenon, known as the "drift barrier," alters the mutation-selection balance in eusocial organisms.

Studies in a range of social arthropods including ants, termites, crustaceans and spiders have shown an elevated ratio of nonsynonymous to synonymous substitutions (dN/dS), indicating relaxed purifying selection due to small Ne. In termite species with complex social structures, such as those with large colonies and high caste specialization, there are reports of higher dN/dS ratios compared to simpler social species. This suggests that higher social complexity, reflected in traits like nesting strategies and developmental pathways, further reduces Ne and the effectiveness of natural selection. 

The authors address these hypotheses by exploring the genomic impact of eusociality in termites (Isoptera) taking two approaches: First, they analyze transcriptome data from 66 Blattodea species and calculate the ratio of non-synonymous to synonymous mutations (dN/dS) as an indicator of natural selection efficiency and effective population size. They analyses reveal an increased dN/dS ratio in termites compared to other Blattodea species, reinforcing the notion that convergent evolution toward eusociality significantly reduces effective population size and weakens natural selection efficiency across the genome. Additionally, a comparison of 68 termite transcriptomes shows that this effect is more pronounced in species with higher social complexity. This is exciting as it advances our understanding of how increasing complexity in social organization decreases Ne and the efficiency of natural selection. The study substantiates the notion that social transitions follow evolutionary trajectories where lower and Ne and increasing drift have negative consequences for genome evolution (Ma et al 2024).

References

Camille Roux, Alice Ha, Arthur Weyna, Morgan Lode, Jonathan Romiguier (2024) The impact of social complexity on the efficacy of natural selection in termites. bioRxiv, ver.2 peer-reviewed and recommended by PCI Evol Biol. https://doi.org/10.1101/2024.04.26.591327

Jilong Ma, Jesper Bechsgaard, Anne Aagaard, Palle Villesen, Trine Bilde, Mikkel Heide Schierup (2024) Sociality in spiders is an evolutionary dead-end. 
bioRxiv 2024.04.22.590577. https://doi.org/10.1101/2024.04.22.590577

The influence of environmental change over geological time on the tempo and mode of biological diversification is a hot topic in biogeography. Of central interest are questions about where, when, and how fast lineages proliferated, suffered extinction, and migrated in response to tectonic events, the waxing and waning of dominant biomes, etc. In this context, the dynamic conditions of the Miocene have received much attention, from studies of many clades and biogeographic regions. Here, Chazot et al. [1] present an exemplary analysis of butterflies (tribe Ithomiini) in the Neotropics, examining their diversification across the Andes and Amazon. They infer sharp contrasts between these regions in the late Miocene: accelerated diversification during orogeny of the Andes, and greater extinction in the Amazon associated during the Pebas system, with interchange and local diversification increasing following the Pebas during the Pliocene.
Two features of this study stand out. First is the impressive taxon sampling (340 out of 393 extant species). Second is the use of ancestral range reconstructions to compute per-lineage rates of colonization between regions, and rates of speciation within regions, through time. The latter allows for relatively fine-grained comparisons across the 2 fundamental dimensions of historical biogeography, space and time, and is key to the main results. The method resonated with me because I performed a similar analysis in a study showing evidence for uplift-driven diversification in the Hengduan Mountains of China [2]. This analysis is complemented by a variety of other comparative methods for inferring variable diversification across clades, through time, and in response to external factors. Overall, it represents a very nice contribution to our understanding of the effects of Miocene/Pliocene environmental change on the evolution of Neotropical biodiversity.

References

[1] Chazot N, Willmott KR, Lamas G, Freitas AVL, Piron-Prunier F, Arias CF, Mallet J, De-Silva DL and Elias M. 2017. Renewed diversification following Miocene landscape turnover in a Neotropical butterfly radiation. BioRxiv 148189, ver 4 of 19th December 2017. doi: 10.1101/148189

[2] Xing Y, and Ree RH. 2017. Uplift-driven diversification in the Hengduan Mountains, a temperate biodiversity hotspot. Proceedings of the National Academy of Sciences of the United States of America, 114: E3444-E3451. doi: 10.1073/pnas.1616063114

Natural populations do not consist of only perfectly adapted individuals. If they did, of course, there would be no fodder for evolution by natural selection. And natural selection is operating all the time, winnowing out less well adapted phenotypes through differential reproduction and survival. Demonstrations of natural selection modifying characters-state distributions to bring phenotypes closer to their optima abound in the evolution literature, with examples of short- and long-term changes in phenotype and allele frequencies.  

However, evolutionary biologists know that populations cannot reach their adaptive peaks. Natural selection is tracking a moving target, always with some generations of lag time. The adaptive landscape is multidimensional, so the optimal combination of multiple character states may be impossible because of constraints and trade-offs. Natural selection does not operate alone or in isolation – new mutations and migrants that were selected under other conditions will inject locally non-adaptive genetic variation and genetic drift can change allele frequencies in random directions. We understand these processes that generate and maintain less advantageous variants on a continuous gradient from an optimal phenotype in a fitness landscape. More puzzling are heritable polymorphisms with distinct morphologies, physiologies or behaviours maintained in populations despite their measurably lower reproductive success. But a complete model of evolution must also be able to accommodate these Darwinian paradoxes.

Raymond et al. (2023) investigate one such Darwinian paradox: In humans, male homosexual mate preference is heritable and is associated with a large reduction in offspring production but nonetheless occurs at relatively high frequencies in most human populations. Furthermore, multiple studies have found that homosexual men come from families that are, on average, larger than those of heterosexual men and that homosexual men have, on average, higher birth rank than do heterosexual men, i.e., having more older siblings and, particularly, more older brothers. Two types of mechanisms consistent with these observations have been proposed: 1) An evolutionary mechanism of sex-antagonistic pleiotropy, whereby highly fecund mothers are more likely to produce homosexual sons, and 2) A mechanistic explanation whereby successive male pregnancies alter the uterine environment by increasing the probability of an immune reaction by the mother to her male fetus, altering development of sexually dimorphic brain structures relevant to sexual orientation.

In this article, the authors explore these two mechanisms of sex-antagonistic effects (AE) and fraternal birth order effects (FBOE) and test how well they account for patterns of male homosexuality in population and family data. Clearly, these two effects are somewhat confounded because high birth ranks can only occur in large families. If, indeed, the probability of male homosexuality increases with increasing numbers of (maternal) older brothers, homosexual males will be more common in larger families. Similarly, if high female fecundity leads to a higher probability of male homosexuality via sex-antagonistic effects, homosexual males will, on average, have more older brothers. To disentangle the actions of these two effects the authors modelled the relationship between birth rank and population fecundity and investigated whether AE or FBOE modified this relationship for homosexual men.  Simulation results were compared with aggregated population data from 13 countries.  Family data on individuals’ sexual preference, birth rank and number of male and female siblings from France, Greece and Indonesia were analysed with generalised linear models and Bayesian approaches to test for a signal of AE or FBOE. 

These analyses revealed a significant older-brother effect (FBOE) explaining patterns of occurrence of homosexuality in population and family data but no significant independent sex-antagonistic effect (AE). Thus larger family sizes of homosexual men appear due to the older-brother effect, with individuals of high birth rank coming necessarily from large sibships. The simulation approach also revealed that modelling a fraternal birth order effect (FBOE), such that individuals with more older brothers are more likely to be homosexual, generates an artefactual older sister effect simply because homosexual men are overrepresented at higher birth ranks. Older-sister effects reported in the literature may, therefore, be statistical artefacts of an underlying older-brother effect.

This paper is interesting for a number of reasons. It does an excellent job of explaining, identifying and dealing with estimation biases and testing for artefactual relationships generated by collinearity. It applies state-of-the art analytical/statistical tools. It breaks down two colinear effects and shows that only one really explains phenotypic variation. This is a great example of how to disentangle correlated variables that may or may not both contribute to trait variation. But most intriguingly, we are left without evidence for an evolutionary mechanism that compensates the large fitness cost associated with male homosexuality in humans. How can we explain high heritability maintained in the face of strong directional selection that should erode heritable genetic variation? The usual suspects include cryptic compensatory mechanisms yet to be discovered or flawed estimates of selection or heritability. For example, data on heritability of male homosexual mate preference in humans come from twin studies and twins share birth rank as well as alleles. Thus it is possible that heritability is over-estimated, including the environmental component associated with birth rank. 

If, as the authors demonstrate here, birth rank is the strongest predictor of male homosexual mate preference, selection may be acting on a non-heritable plastic component of phenotypic variation. This could explain why heritable variation is not exhausted by selection, rendering the paradox less paradoxical, but fails to provide an adaptive explanation for the maintenance of male homosexual mate preference. 

References

Raymond M., Turek D., Durand V., Nila S., Suryobroto B., Vadez J., Barthes J., Apostolou M. and Crochet P.-A. (2023) Increased birth rank of homosexual males: disentangling the older brother effect and sexual antagonism hypothesis. bioRxiv, 2022.02.22.481477, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.02.22.481477

Polyploidy, which results in the presence of more than two sets of homologous chromosomes represents a major feature of plant genomes that have undergone successive rounds of duplication followed by more or less rapid diploidization during their evolutionary history. Polyploid complexes containing diploid and derived polyploid taxa are excellent model systems for understanding the short-term consequences of whole genome duplication, and have been particularly well-explored in evolutionary ecology (Ramsey and Ramsey 2014, Rice et al. 2019). Many polyploids (especially when resulting from interspecific hybridization, i.e. allopolyploids) are successful invaders (te Beest et al. 2012) as a result of rapid genome dynamics, functional novelty, and trait evolution. The origin (parental legacy) and modes of formation of polyploids have a critical impact on the subsequent polyploid evolution. Thus, elucidation of the genomic composition of polyploids is fundamental to understanding trait evolution, and such knowledge is still lacking for many invasive species.

Genus Ludwigia is characterized by a complex taxonomy, with an underexplored evolutionary history. Species from section Jussieae form a polyploid complex with diploids, tetraploids, hexaploids, and decaploids that are notorious invaders in freshwater and riparian ecosystems (Thouvenot et al.2013).   Molecular phylogeny of the genus based on nuclear and chloroplast sequences (Liu et al. 2027) suggested some relationships between diploid and polyploid species, without fully resolving the question of the parentage of the polyploids. In their study, Barloy et al. (2023) have used a combination of molecular cytogenetics (Genomic In situ Hybridization), morphology and experimental crosses to elucidate the genomic compositions of the polyploid species, and show that the examined polyploids are of hybrid origin (allopolyploids). The tetraploid L. stolonifera derives from the diploids L. peploides subsp. montevidensis (AA genome) and L. helminthorhiza (BB genome). The tetraploid L. ascendens also share the BB genome combined with an undetermined different genome. The hexaploid L. grandiflora subsp. grandiflora has inherited the diploid AA genome combined with additional unidentified genomes. The decaploid L. grandiflora subsp. hexapetala has inherited the tetraploid L. stolonifera and the hexaploid L. grandiflora subsp. hexapetala genomes. As the authors point out, further work is needed, including additional related diploid (e.g. other subspecies of L. peploides) or tetraploid (L.  hookeri and L. peduncularis)  taxa that remain to be investigated, to address the nature of the undetermined parental genomes mentioned above. 

The presented work (Barloy et al.  2023) provides significant knowledge of this poorly investigated group with regard to genomic information and polyploid origin, and opens perspectives for future studies. The authors also detect additional diagnostic morphological traits of interest for in-situ discrimination of the taxa when monitoring invasive populations.  

References

Barloy D., Portillo-Lemus L., Krueger-Hadfield S.A., Huteau V., Coriton O. (2024). Genomic relationships among diploid and polyploid species of the genus Ludwigia L. section Jussiaea using a combination of molecular cytogenetic, morphological, and crossing investigations. BioRxiv, ver. 4 peer-reviewed and recommended  by Peer Community in Evolutionary Biology https://doi.org/10.1101/2023.01.02.522458

te Beest M., Le Roux J.J., Richardson D.M., Brysting A.K., Suda J., Kubešová M., Pyšek P. (2012). The more the better? The role of polyploidy in facilitating plant invasions. Annals of Botany, Volume 109, Issue 1 Pages 19–45, https://doi.org/10.1093/aob/mcr277

Ramsey J. and Ramsey T. S. (2014). Ecological studies of polyploidy in the 100 years following its discovery Phil. Trans. R. Soc. B369 1–20  https://doi.org/10.1098/rstb.2013.0352  

Rice, A., Šmarda, P., Novosolov, M. et al. (2019). The global biogeography of polyploid plants. Nat Ecol Evol 3, 265–273. https://doi.org/10.1038/s41559-018-0787-9

Thouvenot L, Haury J, Thiebaut G. (2013). A success story: Water primroses, aquatic plant pests. Aquat. Conserv. Mar. Freshw. Ecosyst. 23:790–803  https://doi.org/10.1002/aqc.2387  

The genomic revolution has given us access to inexpensive genetic data for any species. Simultaneously we have lost the ability to easily identify chimerism in samples or some unusual deviations from standard Mendelian genetics. Methods have been developed to identify sex chromosomes, characterise the ploidy, or understand the exact form of parthenogenesis from genomic data. However, we rarely consider that the tissues we extract DNA from could be a mixture of cells with different genotypes or karyotypes. This can nonetheless happen for a variety of (fascinating) reasons such as somatic chromosome elimination, transmissible cancer, or parental genome elimination. Without a dedicated analysis, it is very easy to miss it.

In this preprint, Jaron et al. (2022) used an ingenious analysis of whole individual NGS data to test the hypothesis of paternal genome elimination in the globular springtail Allacma fusca. The authors suspected that a high fraction of the whole body of males is made of sperm in this species and if this species undergoes paternal genome elimination, we would expect that sperm would only contain maternally inherited chromosomes. Given the reference genome was highly fragmented, they developed a two-tissue model to analyse Kmer spectra and obtained confirmation that around one-third of the tissue was sperm in males. This allowed them to test whether coverage patterns were consistent with the species exhibiting paternal genome elimination. They combined their estimation of the fraction of haploid tissue with allele coverages in autosomes and the X chromosome to obtain support for a bias toward one parental allele, suggesting that all sperm carries the same parental haplotype. It could be the maternal or the paternal alleles, but paternal genome elimination is most compatible with the known biology of Arthropods. SNP calling was used to confirm conclusions based on the analysis of the raw pileups.

I found this study to be a good example of how a clever analysis of Kmer spectra and allele coverages can provide information about unusual modes of reproduction in a species, even though it does not have a well-assembled genome yet. As advocated by the authors, routine inspection of Kmer spectra and allelic read-count distributions should be included in the best practice of NGS data analysis. They provide the method to identify paternal genome elimination but also the way to develop similar methods to detect another kind of genetic chimerism in the avalanche of sequence data produced nowadays.

References

Jaron KS, Hodson CN, Ellers J, Baird SJ, Ross L (2022) Genomic evidence of paternal genome elimination in the globular springtail Allacma fusca. bioRxiv, 2021.11.12.468426, ver. 5 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2021.11.12.468426