Not all genetic elements composing genomes are there for the benefit of their carrier. Many have no consequences on fitness, or too mild ones to be eliminated by selection, and thus stem from neutral processes. Many others are indeed the product of selection, but one acting at a different level, increasing the fitness of some elements of the genome only, at the expense of the “organism” as a whole. These can be called selfish genetic elements, and come into a wide variety of flavours [1], illustrating many possible means to cheat with “fair” reproductive processes such as meiosis, and thus get overrepresented in the offspring of their hosts. Producing copies of itself through transposition is one such strategy; a very successful one indeed, explaining a large part of the genomic content of many organisms. Killing non carrier gametes following meiosis in heterozygous carriers is another one. Less know and less common is the ability of some elements to turn heterozygous carriers into homozygous ones, that will thus transmit the selfish elements to all offspring instead of half. This is achieved by nucleic sequences encoding so-called “Homing endonucleases” (HEs). These proteins tend to induce double strand breaks of DNA specifically in regions homologous to their own insertion sites. The recombination machinery is such that the intact homologous region, that is, the one carrying the HE sequence, is then used as a template for the reparation of the break, resulting in the effective conversion of a non-carrier allele into a carrier allele. Such elements can also occur in the mitochondrial genomes of organisms where mitochondria are not strictly transmitted by one parent only, offering mitochondrial HEs some opportunities for “homing” into new non carrier genomes. This is the case in yeasts, where HEs were first reported [2,3].
In this new study, based on genomic experimental data from the fungal maize pathogen Ustilago maydis, Julien Dutheil and colleagues [4] document one possible evolutionary pathway for which little evidence existed before: the passage of a mitochondrial HE into the nuclear genome. The GC content of this region leaves little doubt on its mitochondrial origin, and homologs can indeed be found in the mitochondrial genomes of close relatives. Strangely enough, U. maydis itself does not appear to carry this selfish element in its own mitochondria, suggesting it may have been acquired from a different species, or be subject to a sufficiently rapid turnover to have been recently lost.
Many elements of the story uncovered by this study remain mysterious. How, in the first place, was this HE gene inserted in a nuclear genomic region that shows no apparent homology with its original insertion site, making typical “homing” a not-so-likely explanation? This question may in fact be generalised to many HE systems: is the first insertion into a homing site always the product of a typical homing event, which implies the presence of an homologous template DNA fragment, or can HE genes insert through other means? But then, why specifically in regions that would be targeted by the nuclease they encode? What is the evolutionary fate of this newly inserted element? The new gene may well be on its way to pseudogenisation, as suggested by the truncation of its upper part, precluding its functioning as a HE, and the lack of evidence of selective constraints through dN/dS analysis; but the mutation generated by the insertion event may have phenotypic implications, possibly through the partial truncation of another gene, encoding a helicase. How old is this insertion? The fact that it has accumulated some mutations makes a very recent event rather unlikely, but this insertion has been detected in only one isolate of U. maydis, suggesting it is not so frequent in natural populations.
Whatever the answers to these open questions, that will hopefully be addressed by further work on this system, the present study has revealed that horizontal transmission enlarges the scope of possible evolutionary consequences of HE genes, that may move not only between mitochondrial genomes, but also occasionally into a nucleus.

References

[1] Burt, A., and Trivers, R. (2006). Genes in Conflict: The Biology of Selfish Genetic Elements. Belknap Press.
[2] Coen, D., Deutch, J., Netter, P., Petrochillo, E., and Slonimski, P. (1970). Mitochondrial genetics. I. Methodology and phenomenology. Symposia of the Society for Experimental Biology, 24, 449-496.
[3] Colleaux, L., D’Auriol, L., Betermier, M., Cottarel, G., Jacquier, A., Galibert, F., and Dujon, B. (1986). Universal code equivalent of a yeast mitochondrial intron reading frame is expressed into E. coli as a specific double strand endonuclease. Cell, 44, 521–533. doi: 10.1016/0092-8674(86)90262-X
[4] Dutheil, J. Y., Münch, K., Schotanus, K., Stukenbrock, E. H., and Kahmann, R. (2020). The insertion of a mitochondrial selfish element into the nuclear genome and its consequences. bioRxiv, 787044, ver. 4 peer-reviewed and recommended by PCI Evolutionary Biology. doi: 10.1101/787044

Flowering plants display a staggering diversity of both mating systems and life histories, ranging from almost exclusively selfers to obligate outcrossers, very short-lived annual herbs to super long lived trees. One pervasive pattern that has attracted considerable attention is the tight correlation that is found between mating systems and lifespan [1]. Until recently, theoretical explanations for these patterns have relied on static models exploring the consequences of several non-mutually exclusive important process: levels of inbreeding depression and ability to successfully were center stage. This make sense: successful colonization after long‐distance dispersal is far more likely to happen for self‐compatible than for self‐incompatible individuals in a sexually reproducing species. Furthermore, inbreeding depression (essentially a genetically driven phenomenon) and reproductive insurance are expected to shape the evolution of both mating system and lifespan.
But modelling jointly several processes and how their interplay to shape the evolution of a trait is challenging enough so models for the evolution of mating system tend invariably – for mathematical convenience and tractability – to fix lifespan [2].
However, comparative analysis of between species variations that map traits transitions among sister species in phylogenetic trees reveals a pervasive pattern: frequent transitions from a state outcrossing perennial to selfing annuals. This beg the question: is one transition triggering the other and if so, what comes first or are these transitions happening together? In this work, Lesaffre and Billiard use a very sophisticated machinery developed by Kirkpatrick et al. [3] and consider a general class of so-called modifiers models [4]. They study jointly the evolution of life span and mating system. They do so by using models where different life stages are tracked with life stage having some (fixed for once) amount of inbreeding depression. Their paper is technically demanding, mixing analytics and computer simulations, and along the way generates several important findings that are expected to stimulate further empirical and theoretical studies: (1) pure selfing versus pure outcrossing is the expected stable evolutionary outcomes (despite observation that mixed mating systems can be regularly met in nature), (2) increasing life-span drastically reduces the scope for the evolution of selfing, conversely (3) transition to selfing will also select for shorter life span as a way to mitigate the cumulative effects of inbreeding depression on adult life stages.
As usual there is room for future work, in particular the authors’ model assumes fixed inbreeding depression in the different life stages and this highlights the need for models that explore how inbreeding depression, a pivotal quantity in these models, can itself be molded by both mating system and lifespan. A third-generation of models should be “soon” on the way!

References
[1] Grossenbacher D, Briscoe Runquist R, Goldberg EE, and Brandvain Y. (2015) Geographic range size is predicted by plant mating system. Ecology Letters 18, 706–713. doi: 10.1111/ele.12449
[2] Morgan MT, Schoen DJ, and Bataillon T. (1997) The evolution of self-fertilization in perennials. The American Naturalist 150, 618–638. doi: 10.1086/286085
[3] Kirkpatrick M, Johnson T, and Barton N. (2002) General models of multilocus evolution. Genetics 161, 1727–1750.
[4] Lesaffre, T, and Billiard S. (2019) The joint evolution of lifespan and self-fertilisation. bioRxiv, 420877, ver. 3 peer-reviewed and recommended by PCI Evol Biol. doi: 10.1101/420877

Sexual selection occurs in flowering plants too. However it tends to be understudied in comparison to animal sexual selection, in part because the minuscule size and long dispersal distances of the individuals producing male gametes (pollen grains) seriously complicate the estimation of male siring success and thereby the measurement of sexual selection. Dorken and Perry [1] introduce a novel and clever approach to estimate sexual selection in plants, which bypasses the need for a direct quantification of absolute male mating success. This approach builds on the fact that the strength of sexual selection is directly related to the ability of individuals to monopolize mates [2]. In plants, mate monopolization can be assessed by examining the proportion of seeds produced by a given plant that are full-sibs, i.e. that share the same father. A nice feature of this proportion of full-sib seeds per maternal parent is it equals the coefficient of correlated paternity of Ritland [3], which can be readily obtained from the hundreds of plant mating system studies using genetic markers. A less desirable feature of the proportion of full sibs per maternal plant is that it is inversely related to population size, an effect that should be corrected for. The resulting index of mate monopolization is a simple product: (coefficient of correlated paternity)x(population size – 1). The authors test whether their index of mate monopolization is a good correlate of sexual selection, measured more traditionally as the selection differential on a trait influencing mating success, using a combination of theoretical and experimental approaches. Both approaches confirm that the two quantities are positively correlated, which suggests that the index of mate monopolization could be a convenient way to estimate the relative strength of sexual selection in flowering plants. These results call for further investigation, e.g. to verify that the effect of population size is well controlled for, or to assess the effects of non-random mating and inbreeding depression; however, this work paves the way for an expansion of sexual selection studies in flowering plants.

References

[1] Dorken ME and Perry LE. 2017. Correlated paternity measures mate monopolization and scales with the magnitude of sexual selection. Journal of Evolutionary Biology 30: 377-387 doi: 10.1111/jeb.13013

[2] Klug H, Heuschele J, Jennions M and Kokko H. 2010. The mismeasurement of sexual selection. Journal of Evolutionary Biology 23:447-462. doi: 10.1111/j.1420-9101.2009.01921.x

[3] Ritland K. 1989. Correlated matings in the partial selfer Mimulus guttatus. Evolution 43:848-859. doi: 10.2307/2409312

Spatial genetic structure, i.e. the non-random spatial distribution of genotypes, arises in populations because of different processes including spatially limited dispersal and selection. Knowledge on the spatial genetic structure of plant populations is important to assess biological parameters such as gene dispersal distances and the potential for local adaptations, as well as for applications in conservation management and breeding. In their work, Niskanen and colleagues demonstrate a multifaceted approach to characterise the spatial genetic structure in two replicate sites of a continuously distributed Scots pine population in South-Eastern Finland. They mapped and assessed the ages of 469 naturally regenerated adults and genotyped them using a SNP array which resulted in 157 325 filtered polymorphic SNPs. Their dataset is remarkably powerful because of the large numbers of both individuals and SNPs genotyped. This made it possible to characterise precisely the decay of genetic relatedness between individuals with spatial distance despite the extensive dispersal capacity of Scots pine through pollen, and ensuing expectations of an almost panmictic population.

The authors’ data analysis was particularly thorough. They demonstrated that two metrics of pairwise relatedness, the genomic relationship matrix (GRM, Yang et al. 2011) and the kinship coefficient (Loiselle et al. 1995) were strongly correlated and produced very similar inference of family relationships: >99% of pairs of individuals were unrelated, and the remainder exhibited 2nd (e.g., half-siblings) to 4th degree relatedness. Pairwise relatedness decayed with spatial distance which resulted in extremely weak but statistically significant spatial genetic structure in both sites, quantified as Sp=0.0005 and Sp=0.0008. These estimates are at least an order of magnitude lower than estimates in the literature obtained in more fragmented populations of the same species or in other conifers. Estimates of the neighbourhood size, the effective number of potentially mating individuals belonging to a within-population neighbourhood (Wright 1946), were relatively large with Nb=1680-3210 despite relatively short gene dispersal distances, σg = 36.5–71.3m, which illustrates the high effective density of the population. 

The authors showed the implications of their findings for selection. The capacity for local adaptation depends on dispersal distances and the strength of the selection coefficient. In the study population, the authors inferred that local adaptation can only occur if environmental heterogeneity occurs over a distance larger than approximately one kilometre (or larger, if considering long-distance dispersal). Interestingly, in Scots pine, no local adaptation has been described on similar geographic scales, in contrast to some other European or Mediterranean conifers (Scotti et al. 2023).

The authors’ results are relevant for the management of conservation and breeding. They showed that related individuals occurred within sites only and that they shared a higher number of rare alleles than unrelated ones. Since rare alleles are enriched in new and recessive deleterious variants, selecting related individuals could have negative consequences in breeding programmes. The authors also showed, in their response to reviewers, that their powerful dataset was not suitable to obtain a robust estimate of effective population size, Ne, based on the linkage disequilibrium method (Do et al. 2014). This illustrated that the estimation of Ne used for genetic indicators supported in international conservation policy (Hoban et al. 2020, CBD 2022) remains challenging in large and continuous populations (see also Santo-del-Blanco et al. 2023, Gargiulo et al. 2024).

References

CBD (2022) Kunming-Montreal Global Biodiversity Framework. https://www.cbd.int/doc/decisions/cop-15/cop-15-dec-04-en.pdf

Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014). NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne ) from genetic data. Molecular Ecology Resources 14: 209–214. https://doi.org/10.1111/1755-0998.12157

Gargiulo R, Decroocq V, González-Martínez SC, Paz-Vinas I, Aury JM, Kupin IL, Plomion C, Schmitt S, Scotti I, Heuertz M (2024) Estimation of contemporary effective population size in plant populations: limitations of genomic datasets. Evolutionary Applications, in press, https://doi.org/10.1101/2023.07.18.549323

Hoban S, Bruford M, D’Urban Jackson J, Lopes-Fernandes M, Heuertz M, Hohenlohe PA, Paz-Vinas I, et al. (2020) Genetic diversity targets and indicators in the CBD post-2020 Global Biodiversity Framework must be improved. Biological Conservation 248: 108654. https://doi.org/10.1016/j.biocon.2020.108654

Loiselle BA, Sork VL, Nason J & Graham C (1995) Spatial genetic structure of a tropical understorey shrub, Psychotria officinalis (Rubiaceae). American Journal of Botany 82: 1420–1425. https://doi.org/10.1002/j.1537-2197.1995.tb12679.x

Santos-del-Blanco L, Olsson S, Budde KB, Grivet D, González-Martínez SC, Alía R, Robledo-Arnuncio JJ (2022). On the feasibility of estimating contemporary effective population size (Ne) for genetic conservation and monitoring of forest trees. Biological Conservation 273: 109704. https://doi.org/10.1016/j.biocon.2022.109704

Scotti I, Lalagüe H, Oddou-Muratorio S, Scotti-Saintagne C, Ruiz Daniels R, Grivet D, et al. (2023) Common microgeographical selection patterns revealed in four European conifers. Molecular Ecology 32: 393-411. https://doi.org/10.1111/mec.16750

Wright S (1946) Isolation by distance under diverse systems of mating. Genetics 31: 39–59. https://doi.org/10.1093/genetics/31.1.39

Yang J, Lee SH, Goddard ME & Visscher PM (2011) GCTA: a tool for genome-wide complex trait analysis. The American Journal of Human Genetics 88: 76–82. https://www.cell.com/ajhg/pdf/S0002-9297(10)00598-7.pdf

How do phenotypic plasticity and adaptive evolution interact in a novel or changing environment? Does evolution by natural selection generally reinforce initially plastic phenotypic responses, or does it instead oppose them? And to what extent does evolution of a trait involve evolution of its plasticity? These questions have lied at the heart of research on phenotypic evolution in heterogeneous environments ever since it was realized that the environment is likely to affect the expression of many (perhaps most) characters of an individual. Importantly, this broad definition of phenotypic plasticity as change in the average phenotype of a given genotype in response to its environment of development (or expression) does not involve any statement about the adaptiveness of the plastic changes. Theory on the evolution of plasticity has devoted much effort to understanding how reaction norm should evolve under different regimes of environmental change in space and time, and depending on genetic constraints on reaction norm shapes. However on an empirically ground, the questions above have mostly been addressed for individual traits, often chosen a priori for their likeliness to exhibit adaptive plasticity, and we still lack more systematic answers. These can be provided by so-called ‘phenomic’ approaches, where a large number of traits are tracked without prior information on their biological or ecological function. A problem is that the number of phenotypic characters that can be measured in an organism is virtually infinite (and to some extent arbitrary), and that scaling issues makes it difficult to compare different sets of traits. Gene-expression levels offer a partial solution to this dilemma, as they can be considered as a very large number of traits (one per typed gene) that can be measured easily and uniformly (fold change in the number of reads in RNAseq). As for any traits, expression levels of different genes may be genetically correlated, to an extent that depends on their regulation mechanism: cis-regulatory sequences that only affect expression of neighboring genes are likely to cause independent gene expression, while more systematic modifiers of expression (e.g. trans-regulators such as transcription factors) may cause correlated genetic responses of the expression of many genes. Huang and Agrawal [1] have studied plasticity and evolution of gene expression level in young larvae of populations of Drosophila melanogaster that have evolved for about 130 generations under either a constant environment (salt or cadmium), or an environment that is heterogeneous in time or space (combining salt and cadmium). They report a wealth of results, of which we summarize the most striking here. First, among genes that (i) were initially highly plastic and (ii) evolved significant divergence in expression levels between constant environment treatments, the evolved divergence is predominantly in the opposite direction to the initial plastic response. This suggests that either plasticity was initially maladaptive, or the selective pressure changed during the evolutionary process (see below). This somewhat unexpected result strikingly mirrors that from a study published last year in Nature [2], where the same pattern was found for responses of guppies to the presence of predators. However, Huang and Agrawal [1] went beyond this study by deciphering the underlying mechanisms in several interesting ways. First, they showed that change in gene expression often occurred at genes close to SNPs with differentiated frequencies across treatments (but not at genes with differentiated SNPs in their coding sequences), suggesting that cis-regulatory sequences are involved. This is also suggested by the fact that changes in gene expression are mostly caused by the increased expression of only one allele at polymorphic loci, and is a first step towards investigating the genetic underpinnings of (co)variation in gene expression levels. Another interesting set of findings concerns evolution of plasticity in treatments with variable environments. To compare the gene-expression plasticity that evolved in these treatments to an expectation, the authors considered that the expression levels in populations maintained for a long time under constant salt or cadmium had reached an optimum. The differences between these expression levels were thus assumed to predict the level of plasticity that should evolve in a heterogeneous environment (with both cadmium and salt) under perfect environmental predictability. The authors showed that plasticity did evolve more in the expected direction in heterogeneous than in constant environments, resulting in better adapted final expression levels across environments. Taken collectively, these results provide an unprecedented set of patterns that are greatly informative on how plasticity and evolution interact in constant versus changing environments. But of course, interpretations in terms of adaptive versus maladaptive plasticity are more challenging, as the authors themselves admit. Even though environmentally determined gene expression is the basic mechanism underlying the phenotypic plasticity of most traits, it is extremely difficult to relate to more integrated phenotypes for which we can understand the selection pressures, especially in multicellular organisms. The authors have recently investigated evolutionary change of quantitative traits in these selected lines, so it might be possible to establish links between reaction norms for macroscopic traits to those for gene expression levels. Such an approach would also involve tracking gene expression throughout life, rather than only in young larvae as done here, thus putting phenotypic complexity back in the picture also for expression levels. Another difficulty is that a plastic response that was originally adaptive may be replaced by an opposite evolutionary response in the long run, without having to invoke initially maladaptive plasticity. For instance, the authors mention the possibility that a generic stress response is initially triggered by cadmium, but is eventually unnecessary and costly after evolution of genetic mechanisms for cadmium detoxification (a case of so-called genetic accommodation). In any case, this study by Huang and Agrawal [1], together with the one by Ghalambor et al. last year [2], reports novel and unexpected results, which are likely to stimulate researchers interested in plasticity and evolution in heterogeneous environments for the years to come.

References

[1] Huang Y, Agrawal AF. 2016. Experimental Evolution of Gene Expression and Plasticity in Alternative Selective Regimes. PLoS Genetics 12:e1006336. doi: 10.1371/journal.pgen.1006336

[2] Ghalambor CK, Hoke KL, Ruell EW, Fischer EK, Reznick DN, Hughes KA. 2015. Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature. Nature 525: 372-375. doi: 10.1038/nature15256