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22 May 2017
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Can Ebola Virus evolve to be less virulent in humans?

A new hypothesis to explain Ebola's high virulence

Recommended by and based on reviews by Virginie Ravigné and François Blanquart


The tragic 2014-2016 Ebola outbreak that resulted in more than 28,000 cases and 11,000 deaths in West Africa [1] has been a surprise to the scientific community. Before 2013, the Ebola virus (EBOV) was known to produce recurrent outbreaks in remote villages near tropical rainforests in Central Africa, never exceeding a few hundred cases with very high virulence. Both EBOV’s ability to circulate for several months in large urban human populations and its important mutation rate suggest that EBOV’s virulence could evolve and to some extent adapt to human hosts [2]. Up to now, the high virulence of EBOV in humans was generally thought to be maladaptive, the virus being adapted to circulating in wild animal populations (e.g. fruit bats [3]). As a logical consequence, EBOV virulence could be expected to decrease during long epidemics in humans. The present paper by Sofonea et al. [4] challenges this view and explores how, given EBOV’s life cycle and known epidemiological parameters, virulence is expected to evolve in the human host during long epidemics. The main finding of the paper is that there is no chance that EBOV’s virulence decreases in the short and long terms. The main underlying mechanism is that EBOV is also transmitted by dead bodies, which limits the cost of virulence. In itself the idea that selection should select for higher virulence in diseases that are also transmitted after host death will sound intuitive for most evolutionary epidemiologists. The accomplishment of the paper is to make a very strong case that the parameter range where virulence could decrease is very small. The paper further provides scientifically grounded arguments in favor of the safe management of corpses. Safe burial of corpses is culturally difficult to impose. The present paper shows that in addition to instantaneously decreasing the spread of the virus, safe burial may limit virulence increase in the short term and favor of less virulent strains in the long term. Altogether these results make a timely and important contribution to the knowledge and understanding of EBOV.


[1] World Health Organization. 2016. WHO: Ebola situation report - 10 June 2016.

[2] Kupferschmidt K. 2014. Imagining Ebola’s next move. Science 346: 151–152. doi: 10.1126/science.346.6206.151

[3] Leroy EM, Kumulungui B, Pourrut X, Rouquet P, Hassanin A, Yaba P, Délicat A, Paweska, Gonzalez JP and Swanepoel R. 2005. Fruit bats as reservoirs of Ebola virus. Nature 438: 575–576. doi: 10.1038/438575a

[4] Sofonea MT, Aldakak L, Boullosa LFVV and Alizon S. 2017. Can Ebola Virus evolve to be less virulent in humans? bioRxiv 108589, ver. 3 of 19th May 2017; doi: 10.1101/108589

Can Ebola Virus evolve to be less virulent in humans?Mircea T. Sofonea, Lafi Aldakak, Luis Fernando Boullosa, Samuel AlizonUnderstanding Ebola Virus (EBOV) virulence evolution is not only timely but also raises specific questions because it causes one pf the most virulent human infections and it is capable of transmission after the death of its host. Using a compartme...Evolutionary EpidemiologyVirginie Ravigné2017-02-15 13:25:58 View
12 Apr 2017
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Genetic drift, purifying selection and vector genotype shape dengue virus intra-host genetic diversity in mosquitoes

Vectors as motors (of virus evolution)

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Many viruses are transmitted by biological vectors, i.e. organisms that transfer the virus from one host to another. Dengue virus (DENV) is one of them. Dengue is a mosquito-borne viral disease that has rapidly spread around the world since the 1940s. One recent estimate indicates 390 million dengue infections per year [1]. As many arthropod-borne vertebrate viruses, DENV has to cross several anatomical barriers in the vector, to multiply in its body and to invade its salivary glands before getting transmissible. As a consequence, vectors are not passive carriers but genuine hosts of the viruses that potentially have important effects on the composition of virus populations and, ultimately, on virus epidemiology and virulence. Within infected vectors, virus populations are expected to acquire new mutations and to undergo genetic drift and selection effects. However, the intensity of these evolutionary forces and the way they shape virus genetic diversity are poorly known.

In their study, Lequime et al. [2] finely disentangled the effects of genetic drift and selection on DENV populations during their infectious cycle within mosquito (Aedes aegypti) vectors. They evidenced that the genetic diversity of viruses within their vectors is shaped by genetic drift, selection and vector genotype. The experimental design consisted in artificial acquisition of purified virus by mosquitoes during a blood meal. The authors monitored the diversity of DENV populations in Ae. aegypti individuals at different time points by high-throughput sequencing (HTS). They estimated the intensity of genetic drift and selection effects exerted on virus populations by comparing the DENV diversity at these sampling time points with the diversity in the purified virus stock (inoculum).

Disentangling the effects of genetic drift and selection remains a methodological challenge because both evolutionary forces operate concomitantly and both reduce genetic diversity. However, selection reduces diversity in a reproducible manner among experimental replicates (here, mosquito individuals): the fittest variants are favoured at the expense of the weakest ones. In contrast, genetic drift reduces diversity in a stochastic manner among replicates. Genetic drift acts equally on all variants irrespectively of their fitness. The strength of genetic drift is frequently evaluated with the effective population size Ne: the lower Ne, the stronger the genetic drift [3]. The estimation of the effective population size of DENV populations by Lequime et al. [2] was based on single-nucleotide polymorphisms (SNPs) that were (i) present both in the inoculum and in the virus populations sampled at the different time points and (ii) that were neutral (or nearly-neutral) and therefore subjected to genetic drift only and insensitive to selection. As expected for viruses that possess small and constrained genomes, such neutral SNPs are extremely rare. Starting from a set of >1800 SNPs across the DENV genome, only three SNPs complied with the neutrality criteria and were enough represented in the sequence dataset for a precise Ne estimation. Using the method described by Monsion et al. [4], Lequime et al. [2] estimated Ne values ranging from 5 to 42 viral genomes (95% confidence intervals ranged from 2 to 161 founding viral genomes). Consequently, narrow bottlenecks occurred at the virus acquisition step, since the blood meal had allowed the ingestion of ca. 3000 infectious virus particles, on average. Interestingly, bottleneck sizes did not differ between mosquito genotypes. Monsion et al.’s [4] formula provides only an approximation of Ne. A corrected formula has been recently published [5]. We applied this exact Ne formula to the means and variances of the frequencies of the three neutral markers estimated before and after the bottlenecks (Table 1 in [2]), and nearly identical Ne estimates were obtained with both formulas.

Selection intensity was estimated from the dN/dS ratio between the nonsynonymous and synonymous substitution rates using the HTS data on DENV populations. DENV genetic diversity increased following initial infection but was restricted by strong purifying selection during virus expansion in the midgut. Again, no differences were detected between mosquito genotypes. However and importantly, significant differences in DENV genetic diversity were detected among mosquito genotypes. As they could not be related to differences in initial genetic drift or to selection intensity, the authors raise interesting alternative hypotheses, including varying rates of de novo mutations due to differences in replicase fidelity or differences in the balancing selection regime. Interestingly, they also suggest that this observation could simply result from a methodological issue linked to the detection threshold of low-frequency SNPs.


[1] Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, Drake JM, et al. 2013. The global distribution and burden of dengue. Nature 496: 504–7 doi: 10.1038/nature12060

[2] Lequime S, Fontaine A, Gouilh MA, Moltini-Conclois I and Lambrechts L. 2016. Genetic drift, purifying selection and vector genotype shape dengue virus intra-host genetic diversity in mosquitoes. PloS Genetics 12: e1006111 doi: 10.1371/journal.pgen.1006111

[3] Charlesworth B. 2009. Effective population size and patterns of molecular evolution and variation. Nature Reviews Genetics 10: 195-205 doi: 10.1038/nrg2526

[4] Monsion B, Froissart R, Michalakis Y and Blanc S. 2008. Large bottleneck size in cauliflower mosaic virus populations during host plant colonization. PloS Pathogens 4: e1000174 doi: 10.1371/journal.ppat.1000174

[5] Thébaud G and Michalakis Y. 2016. Comment on ‘Large bottleneck size in cauliflower mosaic virus populations during host plant colonization’ by Monsion et al. (2008). PloS Pathogens 12: e1005512 doi: 10.1371/journal.ppat.1005512

Genetic drift, purifying selection and vector genotype shape dengue virus intra-host genetic diversity in mosquitoesLequime S, Fontaine A, Gouilh MA, Moltini-Conclois I and Lambrechts LDue to their error-prone replication, RNA viruses typically exist as a diverse population of closely related genomes, which is considered critical for their fitness and adaptive potential. Intra-host demographic fluctuations that stochastically re...Evolutionary Dynamics, Molecular Evolution, Population Genetics / GenomicsFrédéric Fabre2017-04-10 14:26:04 View
03 Apr 2017
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Things softly attained are long retained: Dissecting the Impacts of Selection Regimes on Polymorphism Maintenance in Experimental Spatially Heterogeneous Environments

Experimental test of the conditions of maintenance of polymorphism under hard and soft selection

Recommended by based on reviews by Joachim Hermisson and 2 anonymous reviewers


Theoretical work, initiated by Levene (1953) [1] and Dempster (1955) [2], suggests that within a given environment, the way populations are regulated and contribute to the next generation is a key factor for the maintenance of local adaptation polymorphism. In this theoretical context, hard selection describes the situation where the genetic composition of each population affects its contribution to the next generation whereas soft selection describes the case where the contribution of each population is fixed, whatever its genetic composition. Soft selection is able to maintain polymorphism, whereas hard selection invariably leads to the fixation of one of the alleles. Although the specific conditions (e.g. of migration between populations or drift level) in which this prediction holds have been studied in details by theoreticians, experimental tests have mainly failed, usually leading to the conclusion that the allele frequency dynamics was driven by other mechanisms in the experimental systems and conditions used. Gallet, Froissart and Ravigné [3] have set up a bacterial experimental system which allowed them to convincingly demonstrate that soft selection generates the conditions for polymorphism maintenance when hard selection does not, everything else being equal. The key ingredients of their experimental system are (1) the possibility to accurately produce hard and soft selection regimes when daily transferring the populations and (2) the ability to establish artificial well-characterized reproducible trade-offs. To do so, they used two genotypes resisting each one to one antibiotic and combined, across habitats, low antibiotic doses and difference in medium productivity. The experimental approach contains two complementary parts: the first one is looking at changes in the frequencies of two genotypes, initially introduced at around 50% each, over a small number of generations (ca 40) in different environments and selection regimes (soft/hard) and the second one is convincingly showing polymorphism protection by establishing that in soft selection regimes, the lowest fitness genotype is not eliminated even when introduced at low frequency. In this manuscript, a key point is the dialog between theoretical and experimental approaches. The experiments have been thought and designed to be as close as possible to the situations analysed in theoretical work. For example, the experimental polymorphism protection test (experiment 2) closely matches the equivalent analysis classically performed in theoretical approaches. This close fit between theory and experiment is clearly a strength of this study. This said, the experimental system allowing them to realise this close match also has some limitations. For example, changes in allele frequencies could only be monitored over a quite low number of generations because a longer time-scale would have allowed the contribution of de novo mutations and the likely emergence of a generalist genotype resisting to both antibiotics used to generate the local adaptation trade-offs. These limitations, as well as the actual significance of the experimental tests, are discussed in deep details in the manuscript.


[1] Levene H. 1953. Genetic equilibrium when more than one niche is available. American Naturalist 87: 331–333. doi: 10.1086/281792

[2] Dempster ER. 1955. Maintenance of genetic heterogeneity. Cold Spring Harbor Symposia on Quantitative Biology. 20: 25–32. doi: 10.1101/SQB.1955.020.01.005

[3] Gallet R, Froissart R, Ravigné V. 2017. Things softly attained are long retained: dissecting the impacts of selection regimes on polymorphism maintenance in experimental spatially heterogeneous environments. bioRxiv 100743; doi: 10.1101/100743

Things softly attained are long retained: Dissecting the Impacts of Selection Regimes on Polymorphism Maintenance in Experimental Spatially Heterogeneous EnvironmentsRomain Gallet, Rémy Froissart, Virginie Ravigné<p>Predicting and managing contemporary adaption requires a proper understanding of the determinants of genetic variation. Spatial heterogeneity of the environment may stably maintain polymorphism when habitat contribution to the next generation c...Adaptation, Evolutionary TheoryStephanie Bedhomme2017-01-17 11:06:21 View
31 Mar 2017
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Human adaptation of Ebola virus during the West African outbreak

Ebola evolution during the 2013-2016 outbreak

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The Ebola virus (EBOV) epidemic that started in December 2013 resulted in around 28,000 cases and more than 11,000 deaths. Since the emergence of the disease in Zaire in 1976 the virus had produced a number of outbreaks in Africa but until 2013 the reported numbers of human cases had never risen above 500. Could this exceptional epidemic size be due to the spread of a human-adapted form of the virus?

The large mutation rate of the virus [1-2] may indeed introduce massive amounts of genetic variation upon which selection may act. Several earlier studies based on the accumulation of genome sequences sampled during the epidemic led to contrasting conclusions. A few studies discussed evidence of positive selection on the glycoprotein that may be linked to phenotypic variations on infectivity and/or immune evasion [3-4]. But the heterogeneity in the transmission of some lineages could also be due to environmental heterogeneity and/or stochasticity. Most studies could not rule out the null hypothesis of the absence of positive selection and human adaptation [1-2 and 5].

In a recent experimental study, Urbanowicz et al. [6] chose a different method to tackle this question. A phylogenetic analysis of genome sequences from viruses sampled in West Africa revealed the existence of two main lineages (one with a narrow geographic distribution in Guinea, and the other with a wider geographic distribution) distinguished by a single amino acid substitution in the glycoprotein of the virus (A82V), and of several sub-lineages characterised by additional substitutions. The authors used this phylogenetic data to generate a panel of mutant pseudoviruses and to test their ability to infect human and fruit bat cells. These experiments revealed that specific amino acid substitutions led to higher infectivity of human cells, including A82V. This increased infectivity on human cells was associated with a decreased infectivity in fruit bat cell cultures. Since fruit bats are likely to be the reservoir of the virus, this paper indicates that human adaptation may have led to a specialization of the virus to a new host.

An accompanying paper in the same issue of Cell by Diehl et al. [7] reports results that confirm the trend identified by Urbanowicz et al. [6] and further indicate that the increased infectivity of A82V is specific for primate cells. Diehl et al. [7] also report some evidence for higher virulence of A82V in humans. In other words, the evolution of the virus may have led to higher abilities to infect and to kill its novel host. This work thus confirms the adaptive potential of RNA virus and the ability of Ebola to specialize to a novel host. In this context, the availability of an effective vaccine against the disease is particularly welcome [8].

The study of Urbanowicz et al. [6] is also remarkable because it illustrates the need of experimental approaches for the study of phenotypic variation when inference methods based on phylodynamics fail to extract a clear biological message. The analysis of genomic evolution is still in its infancy and there is a need for new theoretical developments to help detect more rapidly candidate mutations involved in adaptations to new environmental conditions.


[1] Gire, S.K., Goba, A., Andersen, K.G., Sealfon, R.S.G., Park, D.J., Kanneh, L., Jalloh, S., Momoh, M., Fullah, M., Dudas, G., et al. (2014). Genomic surveillance elucidates Ebola virus origin and transmission during the 2014 outbreak. Science 345, 1369–1372. doi: 10.1126/science.1259657
[2] Hoenen, T., Safronetz, D., Groseth, A., Wollenberg, K.R., Koita, O.A., Diarra, B., Fall, I.S., Haidara, F.C., Diallo, F., Sanogo, M., et al. (2015). Mutation rate and genotype variation of Ebola virus from Mali case sequences. Science 348, 117–119. doi: 10.1126/science.aaa5646
[3] Liu, S.-Q., Deng, C.-L., Yuan, Z.-M., Rayner, S., and Zhang, B. (2015). Identifying the pattern of molecular evolution for Zaire ebolavirus in the 2014 outbreak in West Africa. Infection, Genetics and Evolution 32, 51–59. doi: 10.1016/j.meegid.2015.02.024
[4] Holmes, E.C., Dudas, G., Rambaut, A., and Andersen, K.G. (2016). The evolution of Ebola virus: Insights from the 2013–2016 epidemic. Nature 538, 193–200. doi: 10.1038/nature19790
[5] Azarian, T., Lo Presti, A., Giovanetti, M., Cella, E., Rife, B., Lai, A., Zehender, G., Ciccozzi, M., and Salemi, M. (2015). Impact of spatial dispersion, evolution, and selection on Ebola Zaire Virus epidemic waves. Scientific Reports. 5, 10170. doi: 10.1038/srep10170
[6] Urbanowicz, R.A., McClure, C.P., Sakuntabhai, A., Sall, A.A., Kobinger, G., Müller, M.A., Holmes, E.C., Rey, F.A., Simon-Loriere, E., and Ball, J.K. (2016). Human adaptation of Ebola virus during the West African outbreak. Cell 167, 1079–1087. doi: 10.1016/j.cell.2016.10.013
[7] Diehl, W.E., Lin, A.E., Grubaugh, N.D., Carvalho, L.M., Kim, K., Kyawe, P.P., McCauley, S.M., Donnard, E., Kucukural, A., McDonel, P., et al. (2016). Ebola virus glycoprotein with increased infectivity dominated the 2013-2016 epidemic. Cell 167, 1088–1098. doi: 10.1016/j.cell.2016.10.014
[8] Henao-Restrepo, A.M., Camacho, A., Longini, I.M., Watson, C.H., Edmunds, W.J., Egger, M., Carroll, M.W., Dean, N.E., Diatta, I., Doumbia, M., et al. (2016). Efficacy and effectiveness of an rVSV-vectored vaccine in preventing Ebola virus disease: final results from the Guinea ring vaccination, open-label, cluster-randomised trial (Ebola Ça Suffit!). The Lancet 389, 505-518. doi: 10.1016/S0140-6736(16)32621-6

Human adaptation of Ebola virus during the West African outbreakUrbanowicz, R.A., McClure, C.P., Sakuntabhai, A., Sall, A.A., Kobinger, G., Müller, M.A., Holmes, E.C., Rey, F.A., Simon-Loriere, E., and Ball, J.K.The 2013–2016 outbreak of Ebola virus (EBOV) in West Africa was the largest recorded. It began following the cross-species transmission of EBOV from an animal reservoir, most likely bats, into humans, with phylogenetic analysis revealing the co-ci...Adaptation, Evolutionary Epidemiology, Genome Evolution, Genotype-Phenotype, Molecular Evolution, Species interactionsSylvain Gandon2017-03-31 14:20:38 View
16 Mar 2017
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Correlated paternity measures mate monopolization and scales with the magnitude of sexual selection

Measurement of sexual selection in plants made easier

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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.


[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

Correlated paternity measures mate monopolization and scales with the magnitude of sexual selectionDorken, ME and Perry LEIndirect measures of sexual selection have been criticized because they can overestimate the magnitude of selection. In particular, they do not account for the degree to which mating opportunities can be monopolized by individuals of the sex that ...Sexual SelectionEmmanuelle Porcher2017-03-13 23:22:26 View
14 Mar 2017
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Evolution of multiple sensory systems drives novel egg-laying behavior in the fruit pest Drosophila suzukii

A valuable work lying at the crossroad of neuro-ethology, evolution and ecology in the fruit pest Drosophila suzukii

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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.


[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

Evolution of multiple sensory systems drives novel egg-laying behavior in the fruit pest Drosophila suzukiiMarianthi Karageorgi, Lasse B. Bräcker, Sébastien Lebreton, Caroline Minervino, Matthieu Cavey, K.P. Siju, Ilona C. Grunwald Kadow, Nicolas Gompel, Benjamin Prud’hommeThe rise of a pest species represents a unique opportunity to address how species evolve new behaviors and adapt to novel ecological niches. We address this question by studying the egg-laying behavior of Drosophila suzukii, an invasive agricultur...Adaptation, Behavior & Social Evolution, Evo-Devo, Evolutionary Applications, Evolutionary Ecology, Expression Studies, Genotype-Phenotype, Macroevolution, Molecular EvolutionArnaud Estoup2017-03-13 17:42:00 View
24 Jan 2017
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Birth of a W sex chromosome by horizontal transfer of Wolbachia bacterial symbiont genome

A newly evolved W(olbachia) sex chromosome in pillbug!

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In some taxa such as fish and arthropods, closely related species can have different mechanisms of sex determination and in particular different sex chromosomes, which implies that new sex chromosomes are constantly evolving [1]. Several models have been developed to explain this pattern but empirical data are lacking and the causes of the fast sex chromosome turn over remain mysterious [2-4]. Leclerq et al. [5] in a paper that just came out in PNAS have focused on one possible explanation: Wolbachia. This widespread intracellular symbiont of arthropods can manipulate its host reproduction in a number of ways, often by biasing the allocation of resources toward females, the transmitting sex. Perhaps the most spectacular example is seen in pillbugs, where Wolbachia commonly turns infected males into females, thus doubling its effective transmission to grandchildren. Extensive investigations on this phenomenon were initiated 30 years ago in the host species Armadillidium vulgare. The recent paper by Leclerq et al. beautifully validates an hypothesis formulated in these pioneer studies [6], namely, that a nuclear insertion of the Wolbachia genome caused the emergence of new female determining chromosome, that is, a new sex chromosome.

Many populations of A. vulgare are infected by the feminising Wolbachia strain wVulC, where the spread of the bacterium has also induced the loss of the ancestral female determining W chromosome (because feminized ZZ individuals produce females without transmitting any W). In these populations, all individuals carry two Z chromosomes, so that the bacterium is effectively the new sex-determining factor: specimens that received Wolbachia from their mother become females, while the occasional loss of Wolbachia from mothers to eggs allows the production of males. Intriguingly, studies from natural populations also report that some females are devoid both of Wolbachia and the ancestral W chromosome, suggesting the existence of new female determining nuclear factor, the hypothetical “f element”.

Leclerq et al. [5] found the f element and decrypted its origin. By sequencing the genome of a strain carrying the putative f element, they found that a nearly complete wVulC genome got inserted in the nuclear genome and that the chromosome carrying the insertion has effectively become a new W chromosome. The insertion is indeed found only in females, PCRs and pedigree analysis tell. Although the Wolbachia-derived gene(s) that became sex-determining gene(s) remain to be identified among many possible candidates, the genomic and genetic evidence are clear that this Wolbachia insertion is determining sex in this pillbug strain. Leclerq et al. [5] also found that although this insertion is quite recent, many structural changes (rearrangements, duplications) have occurred compared to the wVulC genome, which study will probably help understand which bacterial gene(s) have retained a function in the nucleus of the pillbug. Also, in the future, it will be interesting to understand how and why exactly the nuclear inserted Wolbachia rose in frequency in the pillbug population and how the cytoplasmic Wolbachia was lost, and to tease apart the roles of selection and drift in this event. We highly recommend this paper, which provides clear evidence that Wolbachia has caused sex chromosome turn over in one species, opening the conjecture that it might have done so in many others.


[1] Bachtrog D, Mank JE, Peichel CL, Kirkpatrick M, Otto SP, Ashman TL, Hahn MW, Kitano J, Mayrose I, Ming R, Perrin N, Ross L, Valenzuela N, Vamosi JC. 2014. Tree of Sex Consortium. Sex determination: why so many ways of doing it? PLoS Biology 12: e1001899. doi: 10.1371/journal.pbio.1001899

[2] van Doorn GS, Kirkpatrick M. 2007. Turnover of sex chromosomes induced by sexual conflict. Nature 449: 909-912. doi: 10.1038/nature06178

[3] Cordaux R, Bouchon D, Grève P. 2011. The impact of endosymbionts on the evolution of host sex-determination mechanisms. Trends in Genetics 27: 332-341. doi: 10.1016/j.tig.2011.05.002

[4] Blaser O, Neuenschwander S, Perrin N. 2014. Sex-chromosome turnovers: the hot-potato model. American Naturalist 183: 140-146. doi: 10.1086/674026

[5] Leclercq S, Thézé J, Chebbi MA, Giraud I, Moumen B, Ernenwein L, Grève P, Gilbert C, Cordaux R. 2016. Birth of a W sex chromosome by horizontal transfer of Wolbachia bacterial symbiont genome. Proceeding of the National Academy of Science USA 113: 15036-15041. doi: 10.1073/pnas.1608979113

[6] Legrand JJ, Juchault P. 1984. Nouvelles données sur le déterminisme génétique et épigénétique de la monogénie chez le crustacé isopode terrestre Armadillidium vulgare Latr. Génétique Sélection Evolution 16: 57–84. doi: 10.1186/1297-9686-16-1-57

Birth of a W sex chromosome by horizontal transfer of Wolbachia bacterial symbiont genomeSébastien Leclercq, Julien Thézé, Mohamed Amine Chebbi, Isabelle Giraud, Bouziane Moumen, Lise Ernenwein, Pierre Grève, Clément Gilbert, and Richard CordauxSex determination is an evolutionarily ancient, key developmental pathway governing sexual differentiation in animals. Sex determination systems are remarkably variable between species or groups of species, however, and the evolutionary forces und...Bioinformatics & Computational Biology, Genome Evolution, Molecular Evolution, Reproduction and Sex, Species interactionsGabriel Marais2017-01-13 15:15:51 View
18 Jan 2017
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Associative Mechanisms Allow for Social Learning and Cultural Transmission of String Pulling in an Insect

Culture in Bumblebees

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This is an original paper [1] addressing the question whether cultural transmission occurs in insects and studying the mechanisms of such transmission. Often, culture-like phenomena require relatively sophisticated learning mechanisms, for example imitation and/or teaching. In insects, seemingly complex processes of social information acquisition, can sometimes instead be mediated by relatively simple learning mechanisms suggesting that cultural processes may not necessarily require sophisticated learning abilities.

An important quality of this paper is to describe neatly the experimental protocols used for such typically complex behavioural analyses, providing a detailed understanding of the results while it remains a joy to read. This becomes rare in high impact journals. In a clever experimental design, individual bumblebees are trained to pull an artificial flower from under a Plexiglas table to get access to a reward, by pulling a string attached to the flower. Individuals that have learnt this task are then shown to inexperienced bees while performing this task. This results in a large proportion of the inexperienced observers learning to pull the string and getting access to the reward. Finally, the authors could then document the spread of the string pulling skill amongst other workers in the colony. Even when the originally trained individuals had died, the skill of string-pulling persisted in the colony, as long as they were challenged with the task. This shows that cultural transmission takes place within a colony. The authors provide evidence that the transmission of this behavior among individuals relies on a mix of social learning by local enhancement (bees were attracted to the location where they had observed a demonstrator) and of non-social, individual learning (pulling the string is learned by trial and errors and not by direct imitation of the conspecific). Data also show that simple associative mechanisms are enough and that stimulus enhancement was involved (bees were attracted to the string when its location was concordant with that during prior observation).

The cleverly designed experiments use a paradigm (string-pulling) which has often been used to investigate cognitive abilities in vertebrates. Comparison with such studies indicate that bees, in some aspects of their learning, may not be different from birds, dogs, or apes as they also relied on the perceptual feedback provided by their actions, resulting in target movement to learn string pulling. The results of the study suggest that the combination of relatively simple forms of social learning and trial-and-error learning can mediate the acquisition of new skills and that bumblebees possess the essential cognitive elements for cultural transmission and in a broader sense, that the capacity of culture may be present within most animals.

Can we expect behavioural innovation such as string pulling to occur in nature? Bombus terrestris colonies can reach a total of several hundreds foragers. In the experiments, foragers needed on average 5 rounds of observations with different demonstrators to learn how to pull the string. As individuals forage in a meadow full of flowers and conspecifics, transmission of behavioural innovations by repeated observations shouldn’t strike us as something impossible. Would the behavior survive through the winter? Bumblebee colonies are seasonal in northern areas and in the Mediterranean area but tropical species persists for several years. In seasonal species, all the workers die before winter and only new queens overwinter. So there is no possibility for seasonal foragers to transmit the technique overwinter. Only queens could potentially transmit it to new foragers in spring. However flowers are different in autumn and spring. Therefore, what queens have learnt about flowers in autumn would unlikely be useful in spring (providing that they can remember it). However there is no reason why the technique couldn't be transmitted from a colony to another between spring to autumn. Such transmission of new behaviour would more easily persist in perennial social insect colonies, like honeybees. Importantly, the bees used in these experiments came from a company whose rearing conditions are unknown, and only a few colonies were used for each experiment. As learning ability has a genetic basis [2-3], colonies differ in their ability to learn [4]. In this regard, the authors showed variation between individual bumblebees and between bumblebee colonies in learning ability. Hence, we would wish to know more about the level of genetic diversity in the wild, and of genetic differentiation between tested colonies (were they independent replicates?), to extrapolate the results to what may happen in the wild.

Excitingly, the authors found 2 true innovators among the >400 individuals that were tested at least once for 5 min who would solve such a task without stepwise training or observation of skilled demonstrators, showing that behavioural innovation can occur in very small numbers of individuals, provided that an ecological trigger is provided (food reward). Hence this study shows that all ingredients for the long proposed “social heredity” theory proposed by Baldwin in 1896 are available in this organism, suggesting that social transmission of behavioural innovations could technically act as an additional mechanism for adaptive evolution [5], next to genetic evolution that may take longer to produce adaptive evolution. The question remains whether the behavioural innovations are arising from standing genetic variation in the bees, or do not need a firm genetic background to appear.


[1] Alem S, Perry CJ, Zhu X, Loukola OJ, Ingraham T, Søvik E, Chittka L. 2016. Associative mechanisms allow for social learning and cultural transmission of string pulling in an insect. PloS Biology 14:e1002564. doi: 10.1371/journal.pbio.1002564

[2] Mery F, Kawecki TJ. 2002. Experimental evolution of learning ability in fruit flies. Proceeding of the National Academy of Science USA 99:14274-14279. doi: 10.1073/pnas.222371199

[3] Mery F, Belay AT, So AKC, Sokolowski MB, Kawecki TJ. 2007. Natural polymorphism affecting learning and memory in Drosophila. Proceeding of the National Academy of Science USA 104:13051-13055. doi: 10.1073/pnas.0702923104

[4] Raine NE, Chittka L. 2008. The correlation of learning speed and natural foraging success in bumble-bees. Proceeding of the Royal Society of London 275: 803-808. doi : 10.1098/rspb.2007.1652

[5] Baldwin JM. 1896. A New Factor in Evolution. American Naturalist 30:441-451 and 536-553. doi: 10.1086/276408

Associative Mechanisms Allow for Social Learning and Cultural Transmission of String Pulling in an InsectAlem S, Perry CJ, Zhu X, Loukola OJ, Ingraham T, Søvik E, Chittka LSocial insects make elaborate use of simple mechanisms to achieve seemingly complex behavior and may thus provide a unique resource to discover the basic cognitive elements required for culture, i.e., group-specific behaviors that spread from “inn...Behavior & Social Evolution, Evolutionary Ecology, Non Genetic Inheritance, Phenotypic PlasticityCaroline Nieberding2017-01-18 10:49:03 View
20 Dec 2016
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Experimental Evolution of Gene Expression and Plasticity in Alternative Selective Regimes

Genetic adaptation counters phenotypic plasticity in experimental evolution

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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.


[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

Experimental Evolution of Gene Expression and Plasticity in Alternative Selective RegimesHuang Y, Agrawal AFLittle is known of how gene expression and its plasticity evolves as populations adapt to different environmental regimes. Expression is expected to evolve adaptively in all populations but only those populations experiencing environmental heterog...Adaptation, Experimental Evolution, Expression Studies, Phenotypic PlasticityLuis-Miguel Chevin2016-12-20 09:04:15 View
19 Dec 2016
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Geographic body size variation in the periodical cicadas Magicicada: implications for life cycle divergence and local adaptation

Megacicadas show a temperature-mediated converse Bergmann cline in body size (larger in the warmer south) but no body size difference between 13- and 17-year species pairs

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Periodical cicadas are a very prominent insect group in North America that are known for their large size, good looks, and loud sounds. However, they are probably known best to evolutionary ecologists because of their long juvenile periods of 13 or 17 years (prime numbers!), which they spend in the ground. Multiple related species living in the same area are often coordinated in emerging as adults during the same year, thereby presumably swamping any predators specialized on eating them.
Life history differences between the 13yr and 17yr cicadas are a particular focus of interest. For example, as it takes time to grow large, one would expect 17yr cicadas to be larger than 13yr cicadas on average. Koyama et al. [1] investigate geographic body size clines for 7 species of periodical cicadas in eastern North America, whose phylogenetic relationships are resolved, in a life history context, using an impressively large number of populations (Fig. 1 of [1]). The authors report generally female-biased sexual body size dimorphism (SSD), and (however not for all species) a positive relationship of body size with habitat annual mean temperature taken from weather data and a negative correlation with latitude (Fig. 3 of [1]). The latter is consistent with a converse Bergmann cline. Crucially, body size of two at least partly sympatric 13y & 17y sister species pairs did not differ (by much), contrary to expectation because the 17y species have more time to grow larger. 13y cicadas must therefore generally grow faster (or 17y cicadas slower) to in the end acquire the same (optimal?) body size. The phylogenetically oldest 13y cicada species, however, is larger, suggesting that selection for large (optimal?) body size has relaxed over evolutionary time, for unknown reasons (about which the authors speculate). A mechanistic explanation for this phenomenon is suggested based on the hypothesis that 17y cicadas simply arrest or slow down growth early during their juvenile stage to delay emergence for 4 further years (Fig. 2 of [1]).
We think this is an impressive data set, and the life history question addressed in this prominent insect taxon should appeal to readers generally interested in whole-organism evolution despite being largely descriptive.


[1] Koyama T, Ito H, Kakishima S, Yoshimura J, Cooley JR, Simon C, Sota T. 2015. Geographic body size variation in the periodical cicadas Magicicada: implications for life cycle divergence and local adaptation. Journal of Evolutionary Biology 28:1270-1277. doi: 10.1111/jeb.12653

Geographic body size variation in the periodical cicadas Magicicada: implications for life cycle divergence and local adaptationKoyama T, Ito H, Kakishima S, Yoshimura J, Cooley JR, Simon C, Sota TSeven species in three species groups (Decim, Cassini and Decula) of periodical cicadas (*Magicicada*) occupy a wide latitudinal range in the eastern United States. To clarify how adult body size, a key trait affecting fitness, varies geographical...Adaptation, Evolutionary Ecology, Life History, Macroevolution, Phylogeography & Biogeography, SpeciationWolf Blanckenhorn2016-12-19 10:39:22 View