Koutsovoulos et al. [1] have generated and analysed the first population genomic dataset in root-knot nematode Meloidogyne incognita. Why is this interesting? For two major reasons. First, M. incognita has been documented to be apomictic, i.e., to lack any form of sex. This is a trait of major evolutionary importance, with implications on species adaptive potential. The study of genome evolution in asexuals is fascinating and has the potential to inform on the forces governing the evolution of sex and recombination. Even small amounts of sex, however, are sufficient to restore most of the population genetic properties of true sexuals [2]. Because rare events of sex can remain undetected in the field, to confirm asexuality in M. incognita using genomic data is an important step. The second reason why M. incognita is of interest is that this nematode is one of the most harmful pests currently living on earth. M. incognita feeds on the roots of many cultivated plants, including tomato, bean, and cotton, and has been of major agricultural importance for decades. A number of races were defined based on host specificity. These have played a key role in attempts to control the dynamic of M. incognita populations via crop rotations. Races and management strategies so far lack any genetic basis, hence the second major interest of this study.
The authors newly sequenced the full genome of eleven strains from Brazil and added nine already available samples from Africa and North-America. They report that, in all likelihood, M. incognita is indeed a purely asexual species. This is supported by (i) the confirmation that the genome is in its major part haploid, and (ii) a spectacularly high level of linkage disequilibrium, which does not decline with genetic distance between loci at a 100kb scale. The absence of sex and recombination is associated in M. incognita with a remarkably low amount of genetic diversity - one order of magnitude less than in typical sexual nematodes - and an heavy load of deleterious mutations, as measured by the ratio of non-synonymous (=amino-acid changing) to synonymous (=amino-acid conservative) diversity in coding sequences. The other important result of this study is that the population substructure in M. incognita is in no way related to host races or geography. The tree genetic clusters that are identified include strains from several continents and feeding on a diversity of host plants.
The implications of this work are numerous. First, the results suggest that M. incognita is an ancient asexual. Asexuality, which was here demonstrated via linkage disequilibrium analysis, must be ancient enough for diploidy (or, in this case, maybe triploidy) to have been lost - i.e., formerly homologous chromosomes have accumulated enough mutations to be assembled as distinct entities. So we are not talking about a highly successful clone having recently spread the world - rather a long-term obligate parthenogen. Asexual organisms are deprived of the source of genetic variation offered by recombination, which is why asexuality is thought to be an evolutionary dead-end. Long-term asexuals are uncommon and even the most famous ones, bdelloid rotifers, are suspected to experience between-individual genetic transfers [3]. M. incognita is apparently a true 'evolutionary scandal', and as such deserves particular attention from molecular evolutionary geneticists.
The lack of any host race effect on the genetic diversity of M. incognita is another important finding. So-called 'races' have largely contributed to shape researchers' view of the structure of the species so far. This study demonstrates that a mental effort is now needed to forget about races, and consider host-specificity for what it is - a phenotypic trait. This result implies that many host shifts must have independently occurred in the three M. incognita genetic lineages, suggesting an arms race between plants and nematodes, which in the absence of sex and recombination must be entirely mutation-driven on the nematode side. Genes functionally involved in the arms race might therefore be expected to have experienced convergent evolution, if distinct M. incognita lineages have adopted the same solutions to overcome plant defenses. The present study paves the way for such a genome scan. The authors rightly discuss that the strong adaptive potential of M. incognita, at least in terms of host shift, despite no sex and tiny amounts of genetic diversity, is a paradox that would deserve to be further investigated.

References

[1] Koutsovoulos, G. D., Marques, E., Arguel, M. J., Duret, L., Machado, A. C. Z., Carneiro, R. M. D. G., Kozlowski, D. K., Bailly-Bechet, M., Castagnone-Sereno, P., Albuquerque, E. V., & Danchin, E. G. J. (2019). Population genomics supports clonal reproduction and multiple gains and losses of parasitic abilities in the most devastating nematode plant pest. bioRxiv, 362129, ver. 5, peer-reviewed and recommended by Peer Community in Evolutionary Biology. doi: 10.1101/362129
[2] Hartfield, M. (2016). Evolutionary genetic consequences of facultative sex and outcrossing. Journal of evolutionary biology, 29(1), 5-22. doi: 10.1111/jeb.12770
[3] Debortoli, N., Li, X., Eyres, I., Fontaneto, D., Hespeels, B., Tang, C. Q., Flot, J. F. & Van Doninck, K. (2016). Genetic exchange among bdelloid rotifers is more likely due to horizontal gene transfer than to meiotic sex. Current Biology, 26(6), 723-732. doi: 10.1016/j.cub.2016.01.031

Mutations are the primary source of genetic variation, and there is an obvious interest in characterizing and understanding the processes by which they appear. One particularly important question is the relative abundance, and nature, of replication-dependent and replication-independent mutations - the former arise as cells replicate due to DNA polymerization errors, whereas the latter are unrelated to the cell cycle. A recent experimental study in fission yeast identified a signature of mutations in quiescent (=non-replicating) cells: the spectrum of such mutations is characterized by an enrichment in insertions and deletions (indels) compared to point mutations, and an enrichment of deletions compared to insertions [2].
What Achaz et al. [1] report here is that the very same signature is detectable in humans. This time the approach is indirect and relies on two key aspects of mammalian reproduction biology: (1) oocytes remain quiescent over most of a female's lifespan, whereas spermatocytes keep dividing after male puberty, and (2) X chromosome, Y chromosome and autosomes spend different amounts of time in a female vs. male context. In agreement with the yeast study, Achaz et al. show that in humans the male-associated Y chromosome, for which quiescence is minimal, has by far the lowest ratios of indels to point mutations and of deletions to insertions, whereas the female-associated X chromosome has the highest. This is true both of variants that are polymorphic among humans and of fixed differences between humans and chimpanzees.
So we appear to be here learning about an important and general aspect of the mutation process. The authors suggest that, to a large extent, chromosomes tend to break in pieces at a rate that is proportional to absolute time - because indels in quiescent stage presumably result from double-strand DNA breaks. A very recent analysis of numerous mother-father-child trios in humans confirms this prediction in demonstrating an effect of maternal age, but not of paternal age, on the recombination rate [3]. This result also has important implications with respect to the interpretation of substitution rate variation among taxa and genomic compartments, particularly mitochondrial vs. nuclear, and their relationship with the generation time and longevity of organisms (e.g. [4]).

References

[1] Achaz, G., Gangloff, S., and Arcangioli, B. (2019). The quiescent X, the replicative Y and the Autosomes. BioRxiv, 351288, ver. 3 peer-reviewed and recommended by PCI Evol Biol. doi: 10.1101/351288
[2] Gangloff, S., Achaz, G., Francesconi, S., Villain, A., Miled, S., Denis, C., and Arcangioli, B. (2017). Quiescence unveils a novel mutational force in fission yeast. eLife, 6:e27469. doi: 10.7554/eLife.27469
[3] Halldorsson, B. V., Palsson, G., Stefansson, O. A., Jonsson, H., Hardarson, M. T., Eggertsson, H. P., … Stefansson, K. (2019). Characterizing mutagenic effects of recombination through a sequence-level genetic map. Science, 363: eaau1043. doi: 10.1126/science.aau1043
[4] Saclier, N., François, C. M., Konecny-Dupré, L., Lartillot, N., Guéguen, L., Duret, L., … Lefébure, T. (2019). Life History Traits Impact the Nuclear Rate of Substitution but Not the Mitochondrial Rate in Isopods. Molecular Biology and Evolution, in press. doi: 10.1093/molbev/msy247

Plants display an amazing diversity of reproductive strategies with and without sex. This diversity is particularly remarkable in flowering plants, as highlighted by Charles Darwin, who wrote several botanical books scrutinizing plant reproduction. One particularly influential work concerned floral variation [1]. Darwin recognized that flowers may present different forms within a single population, with or without sex specialization. The number of species concerned is small, but they display recurrent patterns, which made it possible for Darwin to invoke natural and sexual selection to explain them. Most of early evolutionary theory on the evolution of reproductive strategies was developed in the first half of the 20th century and was based on animals. However, the pioneering work by David Lloyd from the 1970s onwards excited interest in the diversity of plant sexual strategies as models for testing adaptive hypotheses and predicting reproductive outcomes [2]. The sex specialization of individual flowers and plants has since become one of the favorite topics of evolutionary biologists. However, attention has focused mostly on cases related to sex differentiation (dioecy and associated conditions [3]). Separate unisexual flower types on the same plant (monoecy and related cases, rendering the plant functionally hermaphroditic) have been much less studied, apart from their possible role in the evolution of dioecy [4] or their association with particular modes of pollination [5].
Two specific non-mutually exclusive hypotheses on the evolution of separate sexes in flowers (dicliny) have been proposed, both anchored in Lloyd’s views and Darwin’s legacy, with selfing avoidance and optimal limited resource allocation. Intermediate sex separation, in which sex morphs have different combinations of unisexual and hermaphrodite flowers, has been crucial for testing these hypotheses through comparative analyses of optimal conditions in suggested transitions. Again, cases in which floral unisexuality does not lead to sex separation have been studied much less than dioecious plants, at both the microevolutionary and macroevolutionary levels. It is surprising that the increasing availability of plant phylogenies and powerful methods for testing evolutionary transitions and correlations have not led to more studies, even though the frequency of monoecy is probably highest among diclinous species (those with unisexual flowers in any distribution among plants within a population [6]).
The study by Torices et al. [7] aims to fill this gap, offering a different perspective to that provided by Diggle & Miller [8] on the evolution of monoecious conditions. The authors use heads of a number of species of the sunflower family (Asteraceae) to test specifically the effect of resource limitation on the expression of sexual morphs within the head. They make use of the very particular and constant architecture of inflorescences in these species (the flower head or “capitulum”) and the diversity of sexual conditions (hermaphrodite, gynomonoecious, monoecious) and their spatial pattern within the flower head in this plant family to develop an elegant means of testing this hypothesis. Their results are consistent with their expectations on the effect of resource limitation on the head, as determined by patterns of fruit size within the head, assuming that female fecundity is more strongly limited by resource availability than male function.
The authors took on a huge challenge in choosing to study the largest plant family (about 25 thousand species). Their sample was limited to only about a hundred species, but species selection was very careful, to ensure that the range of sex conditions and the available phylogenetic information were adequately represented. The analytical methods are robust and cast no doubt on the reported results. However, I can’t help but wonder what would happen if the antiselfing hypothesis was tested simultaneously. This would require self-incompatibility (SI) data for the species sample, as the presence of SI is usually invoked as a powerful antiselfing mechanism, rendering the unisexuality of flowers unnecessary. However, SI is variable and frequently lost in the sunflower family [9]. I also wonder to what extent the very specific architecture of flower heads imposes an idiosyncratic resource distribution that may have fixed these sexual systems in species and lineages of the family. Although not approached in this study, intraspecific variation seems to be low. It would be very interesting to use similar approaches in other plant groups in which inflorescence architecture is lax and resource distribution may differ. A whole-plant approach might be required, rather than investigations of single inflorescences as in this study. This study has no flaws, but instead paves the way for further testing of a long-standing dual hypothesis, probably with different outcomes in different ecological and evolutionary settings. In the end, sex is not only in the head.

References

[1] Darwin, C. (1877). The different forms of flowers on plants of the same species. John Murray.
[2] Barrett, S. C. H., and Harder, L. D. (2006). David G. Lloyd and the evolution of floral biology: from natural history to strategic analysis. In L.D. Harder, L. D., and Barrett, S. C. H. (eds) Ecology and Evolution of Flowers. OUP, Oxford. Pp 1-21.
[3] Geber, M. A., Dawson, T. E., and Delph, L. F. (eds) (1999). Gender and sexual dimorphism in flowering plants. Springer, Berlin.
[4] Charlesworth, D. (1999). Theories of the evolution of dioecy. In Geber, M. A., Dawson T. E. and Delph L. F. (eds) (1999). Gender and sexual dimorphism in flowering plants. Springer, Berlin. Pp. 33-60.
[5] Friedman, J., and Barrett, S. C. (2008). A phylogenetic analysis of the evolution of wind pollination in the angiosperms. International Journal of Plant Sciences, 169(1), 49-58. doi: 10.1086/523365
[6] Renner, S. S. (2014). The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. American Journal of botany, 101(10), 1588-1596. doi: 10.3732/ajb.1400196
[7] Torices, R., Afonso, A., Anderberg, A. A., Gómez, J. M., and Méndez, M. (2019). Architectural traits constrain the evolution of unisexual flowers and sexual segregation within inflorescences: an interspecific approach. bioRxiv, 356147, ver. 3 peer-reviewed and recommended by PCI Evol Biol. doi: 10.1101/356147
[8] Diggle, P. K., and Miller, J. S. (2013). Developmental plasticity, genetic assimilation, and the evolutionary diversification of sexual expression in Solanum. American journal of botany, 100(6), 1050-1060. doi: 10.3732/ajb.1200647
[9] Ferrer, M. M., and Good‐Avila, S. V. (2007). Macrophylogenetic analyses of the gain and loss of self‐incompatibility in the Asteraceae. New Phytologist, 173(2), 401-414. doi: 10.1111/j.1469-8137.2006.01905.x

In this paper, Geoffroy et al. [1] deal with partner choice as a mechanism of maintaining cooperation, and argues that rather than being unequivocally a force towards improved payoffs to everyone through cooperation, partner choice can lead to “over-cooperation” where individuals can evolve to invest so much in cooperation that the costs of cooperating partially or fully negate the benefits from it. This happens when partner choice is consequential and effective, i.e., when interactions are long (so each decision to accept or reject a partner is a bigger stake) and when meeting new partners is frequent when unpaired (so that when one leaves an interaction one can find a new partner quickly). Geoffroy et al. [1] show that this tendency to select for overcooperation under such regimes can be counteracted if individuals base their acceptance-rejection of partners not just on the partner cooperativeness, but also on their own. By using tools from matching theory in economics, they show that plastic partner choice generates positive assortment between cooperativeness of the partners, and in the extreme case of perfectly assortative pairings, makes the pair the unit of selection, which selects for maximum total payoff.
This study is a nice contribution to the literature that illustrates potential complexities with partner choice as a mechanism for cooperation, including how the proximate mechanisms of partner choice can significantly alter the evolutionary trajectory of cooperation. Modeling choice as a reaction norm that depends on one’s own traits also adds a layer of realism to partner choice theory.
The authors are also to be commended for the revisions they made through the review process. Earlier versions of the model somewhat overstated the tendency for fixed partner choice strategies to lead to over cooperation, missing some of the important features in previous models, notably McNamara et al. [2] that can counter this tendency. In this version, the authors acknowledge these factors, mainly, mortality during partner choice (which increases the opportunity cost of forgoing a current partner) and also the fact that endogenous distribution of alternative partners (which will tend to be worse than the overall population distribution, because more cooperative types spend more time attached and less cooperative types more time unattached). These two factors can constrain cooperation from “running away” as the authors put it, but the main point of Geoffroy et al. [1] that plastic choice can create selection against inefficient cooperation stands.
I think the paper will be very stimulating to theoretical and empirical researchers working on partner choice and social behaviors, and happy to recommend it.

References

[1] Geoffroy, F., Baumard, N., & Andre, J.-B. (2019). Why cooperation is not running away. bioRxiv, ver. 5 peer-reviewed and recommended by PCI Evol Biol. doi: 10.1101/316117
[2] McNamara, J. M., Barta, Z., Fromhage, L., & Houston, A. I. (2008). The coevolution of choosiness and cooperation. Nature, 451, 189–192. doi: 10.1038/nature06455

Species everywhere are facing rapid climatic change, and we are increasingly asking whether populations will adapt, shift, or perish [1]. There is a growing realisation that, despite limited within-population genetic variation, many species exhibit substantial geographic variation in climate-relevant traits. This geographic variation might play an important role in facilitating adaptation to climate change [2,3].
Much of our understanding of geographic variation in climate-relevant traits comes from model organisms [e.g. 4]. But as our concern grows, we make larger efforts to understand geographic variation in non-model organisms also. If we understand what adaptive geographic variation exists within a species, we can make management decisions around targeted gene flow [5]. And as empirical examples accumulate, we can look for generalities that can inform management of unstudied species [e.g. 6,7]. Rudin-Bitterli’s paper [8] is an excellent contribution in this direction.
Rudin-Bitterli and her co-authors [8] sampled six frog populations distributed across a strong rainfall gradient. They then assayed these frogs and their offspring for a battery of fitness-relevant traits. The results clearly show patterns consistent with local adaptation to water availability, but they also reveal trade-offs. In their study, frogs from the driest source populations were resilient to the hydric environment: it didn’t really affect them very much whether they were raised in wet or dry environments. By contrast, frogs from wet source areas did better in wet environments, and they tended to do better in these wet environments than did animals from the dry-adapted populations. Thus, it appears that the resilience of the dry-adapted populations comes at a cost: frogs from these populations cannot ramp up performance in response to ideal (wet) conditions.
These data have been carefully and painstakingly collected, and they are important. They reveal not only important geographic variation in response to hydric stress (in a vertebrate), but they also adumbrate a more general trade-off: that the jack of all trades might be master of none. Specialist-generalist trade-offs are often argued (and regularly observed) to exist [e.g. 9,10], and here we see them arise in climate-relevant traits also. Thus, Rudin-Bitterli’s paper is an important piece of the empirical puzzle, and one that points to generalities important for both theory and management.

References

[1] Hoffmann, A. A., and Sgrò, C. M. (2011). Climate change and evolutionary adaptation. Nature, 470(7335), 479–485. doi: 10.1038/nature09670
[2] Aitken, S. N., and Whitlock, M. C. (2013). Assisted Gene Flow to Facilitate Local Adaptation to Climate Change. Annual Review of Ecology, Evolution, and Systematics, 44(1), 367–388. doi: 10.1146/annurev-ecolsys-110512-135747
[3] Kelly, E., and Phillips, B. L. (2016). Targeted gene flow for conservation. Conservation Biology, 30(2), 259–267. doi: 10.1111/cobi.12623
[4] Sgrò, C. M., Overgaard, J., Kristensen, T. N., Mitchell, K. A., Cockerell, F. E., and Hoffmann, A. A. (2010). A comprehensive assessment of geographic variation in heat tolerance and hardening capacity in populations of Drosophila melanogaster from eastern Australia. Journal of Evolutionary Biology, 23(11), 2484–2493. doi: 10.1111/j.1420-9101.2010.02110.x
[5] Macdonald, S. L., Llewelyn, J., and Phillips, B. L. (2018). Using connectivity to identify climatic drivers of local adaptation. Ecology Letters, 21(2), 207–216. doi: 10.1111/ele.12883
[6] Hoffmann, A. A., Chown, S. L., and Clusella‐Trullas, S. (2012). Upper thermal limits in terrestrial ectotherms: how constrained are they? Functional Ecology, 27(4), 934–949. doi: 10.1111/j.1365-2435.2012.02036.x
[7] Araújo, M. B., Ferri‐Yáñez, F., Bozinovic, F., Marquet, P. A., Valladares, F., and Chown, S. L. (2013). Heat freezes niche evolution. Ecology Letters, 16(9), 1206–1219. doi: 10.1111/ele.12155
[8] Rudin-Bitterli, T. S., Evans, J. P., and Mitchell, N. J. (2019). Geographic variation in adult and embryonic desiccation tolerance in a terrestrial-breeding frog. BioRxiv, 314351, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. doi: 10.1101/314351
[9] Kassen, R. (2002). The experimental evolution of specialists, generalists, and the maintenance of diversity. Journal of Evolutionary Biology, 15(2), 173–190. doi: 10.1046/j.1420-9101.2002.00377.x
[10] Angilletta, M. J. J. (2009). Thermal Adaptation: A theoretical and empirical synthesis. Oxford University Press, Oxford.