The total amount of DNA utilized to store hereditary information varies immensely among eukaryotic organisms. Single copy genome sizes – disregarding differences due to ploidy - differ by more than three orders of magnitude ranging from a few million nucleotides (Mb) to hundreds of billions (Gb). With the ever-increasing availability of fully sequenced genomes we now know that most of the difference is due either to whole genome duplication or to variation in the abundance of repetitive elements. Regarding repetitive elements, the evolutionary forces underlying the large variation 'allowing' more or less elements in a genome remain largely elusive. A tentative correlation between an organism's complexity (however this may be adequately measured) and genome size, the so called C-value paradox [1], has long been dismissed. Studies testing for selection on secondary phenotypic effects associated with genome size (cell size, metabolic rates, nutrient availability) have yielded mixed results. Nonadaptive theories capitalizing on a role of deleterious insertion-deletion mutations and genetic drift as the main drivers have likewise received mixed support [2-3]. Overall, most evidence was derived from analyses across broad taxonomical scales [4-6].

Lefébure and colleagues [7] take a different approach. They confine their considerations to a homogeneous, restricted taxonomical group, isopod crustaceans of the superfamily Aselloidea. This taxonomic focus allows the authors to circumvent many of the confounding factors such as phylogenetic inertia, life history divergence and mutation rate variation that tend to trouble analyses across broad taxonomic timescales. Another important feature of the chosen system is the evolutionary independent transition of habitat use that has occurred at least 11 times. One group of species inhabits subterranean ecosystems (groundwater), another group thrives on surface water. Populations of the former live in low-energy habitats and are expected to be outnumbered by their surface dwelling relatives. Interestingly – and a precondition for the study - the groundwater species have significantly larger genomes (up to 137%). With this unique set-up, the authors are able to investigate the link between genome size and evolutionary forces related to a proxy of long-term population size by removing many of the confounding factors a priori.

Upfront, we learn that the dN/dS ratio is higher in the groundwater species. This may either suggest prevalent positive selection or lower efficacy of purifying selection (relaxed constraint) in the group of species in which population sizes are expected to be low. Using a series of population genetic analyses the authors provide compelling evidence for the latter. Analyses are carefully conducted and include models for estimating the intensity and frequency of purifying and positive selection, the DoS (direction of selection) and α statistic. Next the authors also exclude the possibility that increased dN/dS of the subterranean groundwater species may be due to nonfunctionalization, which may result from the subterranean lifestyle.

Overall, these analyses suggest relaxed constraint in smaller populations as the most plausible alternative to explain increased dN/dS ratios. In addition to the efficacy of selection, the authors estimate the timing of the ecological transition under the rationale that the amount of time a species may have been exposed to the subterranean habitat may reflect long term population sizes. To calibrate the 'colonization clock' they apply a neat trick based on the degree of degeneration of the opsin gene (as vision tends to get lost in these habitats). When finally testing which parameters may explain differences in genome size all factors – ecological status, selection efficiency as measured by dN/dS and colonization time - turned out to be significant predictors. Direct estimates of the short term effective population size Ne from polymorphism data, however, did not correlate with genome size. Ruling out the effect of other co-variates such as body size and growth rate the authors conclude that genome size was overall best predicted by long-term population size change upon habitat shift. In that the authors provide convincing evidence that the increase in genome size is linked to a decrease in long-term reduction of selection efficiency of subterranean species. Assuming a bias for insertion mutations over deletion mutations (which is usually the case in eukaryotes) this result is in agreement with the theory of mutational hazard [4-6]. This theory proposed by Michael Lynch postulates that the accumulation of non-functional DNA has a weak deleterious effect that can only be efficiently opposed by natural selection in species with high Ne.

In conclusion, Lefébure and colleagues provide novel and welcome evidence supporting a 'neutralist' hypothesis of genome size evolution without the need to invoke an adaptive component. Methodologically, the study cautions against the common use of polymorphism-based estimates of Ne which are often obfuscated by transitory demographic change. Instead, alternative measures of selection efficacy linked to long-term population size may serve as better predictors of genome size. We hope that this study will stimulate additional work testing the link between Ne and genome size variation in other taxonomical groups [8-9]. Using genome sequences instead of the transcriptome approach applied here may concomitantly further our understanding of the molecular mechanisms underlying genome size change.

References

[1] Thomas, CA Jr. 1971. The genetic organization of chromosomes. Annual Review of Genetics 5: 237–256. doi: 10.1146/annurev.ge.05.120171.001321

[2] Ågren JA, Greiner S, Johnson MTJ, Wright SI. 2015. No evidence that sex and transposable elements drive genome size variation in evening primroses. Evolution 69: 1053–1062. doi: 10.1111/evo.12627

[3] Bast J, Schaefer I, Schwander T, Maraun M, Scheu S, Kraaijeveld K. 2016. No accumulation of transposable elements in asexual arthropods. Molecular Biology and Evolution 33: 697–706. doi: 10.1093/molbev/msv261

[4] Lynch M. 2007. The Origins of Genome Architecture. Sinauer Associates.

[5] Lynch M, Bobay LM, Catania F, Gout JF, Rho M. 2011. The repatterning of eukaryotic genomes by random genetic drift. Annual Review of Genomics and Human Genetics 12: 347–366. doi: 10.1146/annurev-genom-082410-101412

[6] Lynch M, Conery JS. 2003. The origins of genome complexity. Science 302: 1401–1404. doi: 10.1126/science.1089370

[7] Lefébure T, Morvan C, Malard F, François C, Konecny-Dupré L, Guéguen L, Weiss-Gayet M, Seguin-Orlando A, Ermini L, Der Sarkissian C, Charrier NP, Eme D, Mermillod-Blondin F, Duret L, Vieira C, Orlando L, and Douady CJ. 2017. Less effective selection leads to larger genomes. Genome Research 27: 1016-1028. doi: 10.1101/gr.212589.116

[8] Lower SS, Johnston JS, Stanger-Hall KF, Hjelmen CE, Hanrahan SJ, Korunes K, Hall D. 2017. Genome size in North American fireflies: Substantial variation likely driven by neutral processes. Genome Biolology and Evolution 9: 1499–1512. doi: 10.1093/gbe/evx097

[9] Sessegolo C, Burlet N, Haudry A. 2016. Strong phylogenetic inertia on genome size and transposable element content among 26 species of flies. Biology Letters 12: 20160407. doi: 10.1098/rsbl.2016.0407

A classic problem in evolutionary biology is to understand the genetic variance in fitness. The simplest hypothesis is that variation exists, even in well-adapted populations, as a result of the balance between mutational input and selective elimination. This variation causes a reduction in mean fitness, known as the mutation load. Though mutation load is difficult to quantify empirically, indirect evidence of segregating genetic variation in fitness is often readily obtained by comparing the fitness of inbred and outbred offspring, i.e., by measuring inbreeding depression. Mutation-selection balance models have been studied as a means of understanding the genetic variance in fitness, mutation load, and inbreeding depression. Since their inception, such models have increased in sophistication, allowing us to ask these questions under more realistic and varied scenarios. The new theoretical work by Abu Awad and Roze [1] is a substantial step forward in understanding how arbitrary levels of self-fertilization affect variation, load and inbreeding depression under mutation-selection balance.
It has never been entirely clear how selfing should affect these population genetic properties in a multi-locus model. From the single-locus perspective, selfing increases homozygosity, which allows for more efficient purging leading to a prediction of less variance and lower load. On the other hand, selfing directly and indirectly affects several types of multilocus associations, which tend to make selection less efficient. Though this is certainly not the first study to consider mutation-selection balance in species with selfing (e.g., [2-5]), it is perhaps the most biologically realistic. The authors consider a model where n traits are under stabilizing selection and where each locus affects an arbitrary subset of these traits. As others have argued [6-7], this type of fitness landscape model “naturally” gives rise to dominance and epistatic effects. Abu Awad and Roze [1] thoroughly investigate this model both with analytical approximations and stochastic simulations (incorporating the effects of drift).
Their analysis reveals three major parameter regimes. The first regime occurs under low mutation rates, when segregating deleterious alleles are sufficiently rare across the genome that multi-locus genetic associations (disequilibria) can be ignored. As expected, in this regime, increased selfing facilitates purging, thereby leading to less standing genetic variation, lower load and less inbreeding depression.
In the second regime, mutation rates are higher and segregating deleterious alleles are more common. Though the effects of multilocus genetic associations cannot be ignored, Abu Awad and Roze [1] show that a good approximation can be obtained by considering only two-locus associations (ignoring the multitude of higher order associations). This is where the sophistication of their analysis yields the greatest insights. Their analysis shows that two different types of interlocus associations are important. First, selfing directly generates identity disequilibrium (correlation in homozygosity between two loci) that occurs because individuals produced through outbreeding tend to be heterozygous across multiple loci whereas individuals produced by selfing tend to be homozygous across multiple loci. These correlations reduce the efficiency of selection when deleterious effects are partially recessive [5]. Second, selfing indirectly affects traditional linkage disequilibrium. Epistatic selection resulting from the fitness landscape generates negative linkage disequilibrium between alleles at different loci that cause the same direction of deviation in a trait from its optimum. Because selfing reduces the effective rate of recombination, linkage disequilibrium reaches higher levels. Because selection tends to generate compensatory combinations of alleles, partially masking their deleterious effects, these associations also make purging less efficient. Their analysis shows the strength of the effect from identity disequilibrium scales with U, the genome-wide rate of deleterious mutations, but the effect of linkage disequilibrium scales with U/n because with more traits (higher n) two randomly chosen alleles are less likely to affect the same trait and so be subject to epistatic selection. Together, the effects of multilocus associations increase the load and can, in some cases, cause the load to increase as selfing increase from moderate to high levels.
However, their analytical approximations become inaccurate under conditions when the number of epistatically interacting segregating mutations (proportional to U/n) becomes large relative to the effective recombination rate (dependent on outcrossing and recombination rates). In this third regime, higher order genetic associations become important. In the limit of no recombination, model behaves as if the whole genome is a single locus with a very large number of alleles, becoming equivalent to previous studies [2-3].
The study by Abu Awad and Roze [1] helps us better understand the “simplest” explanation for genetic variance in fitness—mutation-selection balance—in a model of considerable complexity involving multiple traits under stabilizing selection, which ‘naturally’ allows for pleiotropy and epistasis. Their model tends to confirm the classic prediction of lower variation in fitness, less load, and inbreeding depression in species with higher levels of selfing. However, their careful analysis provides a clearer picture of how (and by how much) epistasis and selfing affect key population genetic properties.

References

[1] Abu Awad D and Roze D. 2017. Effects of partial selfing on the equilibrium genetic variance, mutation load and inbreeding depression under stabilizing selection. bioRxiv, 180000, ver. 4 of 17th November 2017. doi: 10.1101/180000

[2] Lande R. 1977. The influence of the mating system on the maintenance of genetic variability in polygenic characters. Genetics 86: 485–498.

[3] Charlesworth D and Charlesworth B. 1987. Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics. 18: 237–268. doi: 10.1111/10.1146/annurev.es.18.110187.001321

[4] Lande R and Porcher E. 2015. Maintenance of quantitative genetic variance under partial self-fertilization, with implications for the evolution of selfing. Genetics 200: 891–906. doi: 10.1534/genetics.115.176693

[5] Roze D. 2015. Effects of interference between selected loci on the mutation load, inbreeding depression, and heterosis. Genetics 201: 745–757. doi: 10.1534/genetics.115.178533

[6] Martin G and Lenormand T. 2006. A general multivariate extension of Fisher's geometrical model and the distribution of mutation fitness effects across species. Evolution 60: 893–907. doi: 10.1111/j.0014-3820.2006.tb01169.x

[7] Martin G, Elena SF and Lenormand T. 2007. Distributions of epistasis in microbes fit predictions from a fitness landscape model. Nature Genetics 39: 555–560. doi: 10.1038/ng1998

It is a classical result in the virulence evolution literature that treatments decreasing parasite replication within the host should select for higher replication rates, thus driving increased levels of virulence if the two are correlated. There is some evidence for this in vitro but very little in the field. HIV infections in humans offer a unique opportunity to go beyond the simple predictions that treatments should favour more virulent strains because many details of this host-parasite system are known, especially the link between set-point virus load, transmission rate and virulence.

To tackle this question, Herbeck et al. [1] used a detailed individual-based model. This is original because it allows them to integrate existing knowledge from the epidemiology and evolution of HIV (e.g. recent estimates of the ‘heritability’ of set-point virus load from one infection to the next). This detailed model allows them to formulate predictions regarding the effect of different treatment policies; especially regarding the current policy switch away from treatment initiation based on CD4 counts towards universal treatment.

The results show that, perhaps as expected from the theory, treatments based on the level of remaining host target cells (CD4 T cells) do not affect virulence evolution because they do not strongly affect the virulence level that maximizes HIV’s transmission potential. However, early treatments can lead to moderate increase in virulence within several years if coverage is high enough. These results seem quite robust to variation of all the parameters in realistic ranges.

The great step forward in this model is the ability to obtain quantitative prediction regarding how a virus may evolve in response to public health policies. Here the main conclusion is that given our current knowledge in HIV biology, the risk of virulence evolution is perhaps more limited than expected from a direct application of virulence evolution model. Interestingly, the authors also conclude that recently observed increased in HIV virulence [2-3] cannot be explained by the impact of antiretroviral therapy alone; which raises the question about the main mechanism behind this increase. Finally, the authors make the interesting suggestion that “changing virulence is amenable to being monitored alongside transmitted drug resistance in sentinel surveillance”.

References

[1] Herbeck JT, Mittler JE, Gottlieb GS, Goodreau SM, Murphy JT, Cori A, Pickles M, Fraser C. 2016. Evolution of HIV virulence in response to widespread scale up of antiretroviral therapy: a modeling study. Virus Evolution 2:vew028. doi: 10.1093/ve/vew028

[2] Herbeck JT, Müller V, Maust BS, Ledergerber B, Torti C, et al. 2012. Is the virulence of HIV changing? A meta-analysis of trends in prognostic markers of HIV disease progression and transmission. AIDS 26:193-205. doi: 10.1097/QAD.0b013e32834db418

[3] Pantazis N, Porter K, Costagliola D, De Luca A, Ghosn J, et al. 2014. Temporal trends in prognostic markers of HIV-1 virulence and transmissibility: an observational cohort study. Lancet HIV 1:e119-26. doi: 10.1016/s2352-3018(14)00002-2

Adaptations to a new ecological niche allow species to access new resources and circumvent competitors and are hence obvious pathways of evolutionary success. The evolution of agricultural pest species represents an important case to study how a species adapts, on various timescales, to a novel ecological niche. Among the numerous insects that are agricultural pests, the ability to lay eggs (or oviposit) in ripe fruit appears to be a recurrent scenario. Fruit flies (family Tephritidae) employ this strategy, and include amongst their members some of the most destructive pests (e.g., the olive fruit fly Bactrocera olea or the medfly Ceratitis capitata). In their ms, Karageorgi et al. [1] studied how Drosophila suzukii, a new major agricultural pest species that recently invaded Europe and North America, evolved the novel behavior of laying eggs into undamaged fresh fruit. The close relatives of D. suzukii lay their eggs on decaying plant substrates, and thus this represents a marked change in host use that links to substantial economic losses to the fruit industry. Although a handful of studies have identified genetic changes causing new behaviors in various species, the question of the evolution of behavior remains a largely uncharted territory. The study by Karageorgi et al. [1] represents an original and most welcome contribution in this domain for a non-model species. Using clever behavioral experiments to compare D. suzukii to several related Drosophila species, and complementing those results with neurogenetics and mutant analyses using D. suzukii, the authors nicely dissect the sensory changes at the origin of the new egg-laying behavior. The experiments they describe are easy to follow, richly illustrate through figures and images, and particularly well designed to progressively decipher the sensory bases driving oviposition of D. suzukii on ripe fruit. Altogether, Karageorgi et al.’s [1] results show that the egg-laying substrate preference of D. suzukii has considerably evolved in concert with its morphology (especially its enlarged, serrated ovipositor that enables females to pierce the skin of many ripe fruits). Their observations clearly support the view that the evolution of traits that make D. suzukii an agricultural pest included the modification of several sensory systems (i.e. mechanosensation, gustation and olfaction). These differences between D. suzukii and its close relatives collectively underlie a radical change in oviposition behavior, and were presumably instrumental in the expansion of the ecological niche of the species. The authors tentatively propose a multi-step evolutionary scenario from their results with the emergence of D. suzukii as a pest species as final outcome. Such formalization represents an interesting evolutionary model-framework that obviously would rely upon further data and experiments to confirm and refine some of the evolutionary steps proposed, especially the final and recent transition of D. suzukii from non-invasive to invasive species.

References

[1] Karageorgi M, Bräcker LB, Lebreton S, Minervino C, Cavey M, Siju KP, Grunwald Kadow IC, Gompel N, Prud’homme B. 2017. Evolution of multiple sensory systems drives novel egg-laying behavior in the fruit pest Drosophila suzukii. Current Biology, 27: 1-7. doi: 10.1016/j.cub.2017.01.055

Nobody can ignore that a full understanding of evolution requires an integrated approach from both conceptual and methodological viewpoints. Although some life-history traits, e.g. flowering time, have long been receiving more attention than others, in many cases because the former are more workable than the latter, we must acknowledge that our comprehension about how evolution works is strongly biased and limited. In the Arabidopsis community, such an integration is making good progress as an increasing number of research groups worldwide are changing the way in which evolution is put to the test.

This manuscript [1] is a good example of that as the authors raise an important issue in evolutionary biology by combining gene expression and flowering time data from different sources. In particular, the authors explore how variation in flowering time, which determines lifespan, and host immunity defenses co-vary, which is interpreted in terms of co-evolution between the two traits. Interestingly, the authors go beyond that pattern by separating lifespan-dependent from lifespan–independent defense genes, and by showing that defense genes with variants known to impact fitness in the field are among the genes whose expression co-varies most strongly with flowering time. Finally, these results are supported by a simple mathematical model indicating that such a relationship can also be expected theoretically.

Overall, the readers will find many conceptual and methodological elements of interest in this manuscript. The idea that evolution is better understood under the scope of life history variation is really exciting and challenging, and in my opinion on the right track for disentangling the inherent complexities of evolutionary research. However, only when we face complexity, we also face its costs and burdens. In this particular case, the well-known co-variation between seed dormancy and flowering time is a missing piece, as well as the identification of (variation in) putative selective pressures accounting for the co-evolution between defense mechanisms and life history (seed dormancy vs. flowering time) along environmental gradients. More intellectual, technical and methodological challenges that with no doubt are totally worth it.

Reference

[1] Glander S, He F, Schmitz G, Witten A, Telschow A, de Meaux J. 2017. Assortment of flowering time and defense alleles in natural Arabidopsis thaliana populations suggests co-evolution between defense and vegetative lifespan strategies. bioRxiv ver.1 of June 19, 2017. doi: 10.1101/131136