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07 Jul 2017
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Negative frequency-dependent selection is frequently confounding

Unmasking the delusive appearance of negative frequency-dependent selection

Recommended by based on reviews by David Baltrus and 2 anonymous reviewers

Explaining the processes that maintain polymorphisms in a population has been a fundamental line of research in evolutionary biology. One of the main mechanisms identified that preserves genetic diversity is negative frequency-dependent selection (NFDS), which constitutes a powerful framework for interpreting the presence of persistent polymorphisms. Nevertheless, a number of patterns that are often explained by invoking NFDS may also be compatible with, and possibly more easily explained by, different processes.
In the present manuscript [1], Brisson acknowledges first that genuine NFDS has been instrumental for our understanding on the dynamics that perpetuate polymorphisms, and that the power and importance of NFDS cannot be disregarded. Second, the author aims at identifying certain of the processes that may result in maintenance of genetic diversity, and whose outcome may be mistaken for NFDS, namely directional selection in changing environments, density-dependent fitness, multiple niche selection and community diversity. The author claims that systematic resort to NFDS as explanatory device may have lead to its application to systems where it does not apply or that do not fulfil the basic assumptions of NFDS. The author struggles in the text to provide with a precise, verbal definition of NFDS, and the exchanges with the reviewers during the recommendation process show that agreeing on such a verbal definition of NFDS is not trivial. Probably a profound mathematical formulation of the varying value of a genotype’s fitness relative to other competing ones as a function of their frequency (developing further the synthesis by Heino [2]) may still be wanting. Indeed, the text is intended for a broad audience of evolutionary biologists with operational mathematical knowledge and interest in models, rather than for modellers or biomathematicians. Nevertheless, the manuscript is rich in references to original literature, elaborates on interesting lines of thought and discussion and will hopefully trigger novel experimental and formal research to clarify the role of NFDS and to discern between alternative mechanisms that may render similar patterns of maintenance of genetic diversity.

References

[1] Brisson D. 2017. Negative frequency-dependent selection is frequently confounding. bioRxiv 113324, ver. 3 of 20th June 2017. doi: 10.1101/113324

[2] Heino M, Metz JAJ and Kaitala V. 1998. The enigma of frequency-dependent selection. Trends in Ecology & Evolution 13: 367-370. doi: 1016/S0169-5347(98)01380-9

Negative frequency-dependent selection is frequently confoundingDustin BrissonThe existence of persistent genetic variation within natural populations presents an evolutionary problem as natural selection and genetic drift tend to erode genetic diversity. Models of balancing selection were developed to account for the high ...Evolutionary Applications, Evolutionary Theory, Population Genetics / GenomicsIgnacio Bravo2017-03-03 18:46:42 View
12 Jun 2017
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Evolution and manipulation of vector host choice

Modelling the evolution of how vector-borne parasites manipulate the vector's host choice

Recommended by ORCID_LOGO based on reviews by Samuel Alizon and Nicole Mideo

Many parasites can manipulate their hosts, thus increasing their transmission to new hosts [1]. This is particularly the case for vector-borne parasites, which can alter the feeding behaviour of their hosts. However, predicting the optimal strategy is not straightforward because three actors are involved and the interests of the parasite may conflict with that of the vector. There are few models that consider the evolution of host manipulation by parasites [but see 2-4], but there are virtually none that investigated how parasites can manipulate the host choice of vectors. Even on the empirical side, many aspects of this choice remain unknown. Gandon [5] develops a simple evolutionary epidemiology model that allows him to formulate clear and testable predictions. These depend on which actor controls the trait (the vector or the parasite) and, when there is manipulation, whether it is realised via infected hosts (to attract vectors) or infected vectors (to change host choice). In addition to clarifying the big picture, Gandon [5] identifies some nice properties of the model, for instance an independence of the density/frequency-dependent transmission assumption or a backward bifurcation at R0=1, which suggests that parasites could persist even if their R0 is driven below unity. Overall, this study calls for further investigation of the different scenarios with more detailed models and experimental validation of general predictions.

References

[1] Hughes D, Brodeur J, Thomas F. 2012. Host manipulation by parasites. Oxford University Press.

[2] Brown SP. 1999. Cooperation and conflict in host-manipulating parasites. Proceedings of the Royal Society of London B: Biological Sciences 266: 1899–1904. doi: 10.1098/rspb.1999.0864

[3] Lion S, van Baalen M, Wilson WG. 2006. The evolution of parasite manipulation of host dispersal. Proceedings of the Royal Society of London B: Biological Sciences. 273: 1063–1071. doi: 10.1098/rspb.2005.3412

[4] Vickery WL, Poulin R. 2010. The evolution of host manipulation by parasites: a game theory analysis. Evolutionary Ecology 24: 773–788. doi: 10.1007/s10682-009-9334-0

[5] Gandon S. 2017. Evolution and manipulation of vector host choice. bioRxiv 110577, ver. 3 of 7th June 2017. doi: 10.1101/110577

Evolution and manipulation of vector host choiceSylvain GandonThe transmission of many animal and plant diseases relies on the behavior of arthropod vectors. In particular, the choice to feed on either infected or uninfected hosts can dramatically affect the epidemiology of vector-borne diseases. I develop a...Evolutionary Ecology, Evolutionary Epidemiology, Evolutionary TheorySamuel Alizon2017-03-03 19:18:54 View
12 Jul 2017
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Despite reproductive interference, the net outcome of reproductive interactions among spider mite species is not necessarily costly

The pros and cons of mating with strangers

Recommended by based on reviews by Joël Meunier and Michael D Greenfield

 

Interspecific matings are by definition rare events in nature, but when they occur they can be very important, and not only because they might condition gene flow between species. Even when such matings have no genetic consequence, for instance if they do not yield any fertile hybrid offspring, they can still have an impact on the population dynamics of the species involved [1]. Such atypical pairings between heterospecific partners are usually regarded as detrimental or undesired; as they interfere with the occurrence or success of intraspecific matings, they are expected to cause a decline in absolute fitness.
The story is not always so simple however, and it might all depend on the timing of events and on the identity of the partners. Using the herbivorous mite Tetranychus urticae as a model, Clemente et al. [2] experimentally arranged matings with two other Tetranychus species that commonly share the same host plants as T. urticae. They carefully controlled the history of events: heterospecific matings could occur just before, just after, 24h before, or 24h after, a conspecific mating. Interestingly, the oviposition rate (total fecundity) of females was increased when mating with a heterospecific individual. This suggests that heterospecic sperm can stimulate oogenesis just as conspecific sperm does. Such a positive effect was observed for matings involving T. ludeni females and T. urticae males, but a negative effect is found in the interaction with T. evansi. Sex-ratio (fertilization success in those species) could also be impacted but, unlike fertilization, this occurred when the mating events were distant in time. This is is at odds with what is observed in conspecific matings, where sperm displacement occurs only if mating events are temporally close. Overall, the effects of heterospecific mating were quite variable and it is challenging to predict a single, general, effect of interspecific matings. The net effect will likely be context-dependent, depending on the relative frequency of the difference mating sequences and on how fecundity and sex-ratio contribute to overall fitness, both aspect strongly influenced by the population dynamics and structure.

References

[1] Gröning J. & Hochkirch A. 2008. Reproductive interference between animal species. The Quarterly Review of Biology 83: 257-282. doi: 10.1086/590510

[2] Clemente SH, Santos I, Ponce AR, Rodrigues LR, Varela SAM & Magalhaes S. 2017 Despite reproductive interference, the net outcome of reproductive interactions among spider mite species is not necessarily costly. bioRxiv 113274, ver. 4 of the 30th of June 2017. doi: 10.1101/113274

Despite reproductive interference, the net outcome of reproductive interactions among spider mite species is not necessarily costlySalomé H. Clemente, Inês Santos, Rita Ponce, Leonor R. Rodrigues, Susana A. M. Varela and Sara MagalhãesReproductive interference is considered a strong ecological force, potentially leading to species exclusion. This supposes that the net effect of reproductive interactions is strongly negative for one of the species involved. Testing this requires...Behavior & Social Evolution, Evolutionary Ecology, Species interactionsVincent Calcagno2017-03-06 11:48:08 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.

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

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
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.

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

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
31 Jan 2018
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Identifying drivers of parallel evolution: A regression model approach

A new statistical tool to identify the determinant of parallel evolution

Recommended by based on reviews by Bastien Boussau and 1 anonymous reviewer

In experimental evolution followed by whole genome resequencing, parallel evolution, defined as the increase in frequency of identical changes in independent populations adapting to the same environment, is often considered as the product of similar selection pressures and the parallel changes are interpreted as adaptive.
However, theory predicts that heterogeneity both in mutation rate and selection intensity across the genome can trigger patterns of parallel evolution. It is thus important to evaluate and quantify the contribution of both mutation and selection in determining parallel evolution to interpret more accurately experimental evolution genomic data and also potentially improve our capacity to predict the genes that will respond to selection.
In their manuscript, Bailey, Guo and Bataillon [1] derive a framework of statistical models to partition the role of mutation and selection in determining patterns of parallel evolution at the gene level. The rationale is to use the synonymous mutations dataset as a baseline to characterize the mutation rate heterogeneity, assuming a negligible impact of selection on synonymous mutations and then analyse the non-synonymous dataset to identify additional source(s) of heterogeneity, by examining the proportion of the variation explained by a number of genomic variables.
This framework is applied to a published data set of resequencing of 40 Saccharomyces cerevisiae populations adapting to a laboratory environment [2]. The model explaining at best the synonymous mutations dataset is one of homogeneous mutation rate along the genome with a significant positive effect of gene length, likely reflecting variation in the size of the mutational target. For the non-synonymous mutations dataset, introducing heterogeneity between sites for the probability of a change to increase in frequency is improving the model fit and this heterogeneity can be partially explained by differences in gene length, recombination rate and number of functional protein domains.
The application of the framework to an experimental data set illustrates its capacity to disentangle the role of mutation and selection and to identify genomic variables explaining heterogeneity in parallel evolution probability but also points to potential limits, cautiously discussed by the authors: first, the number of mutations in the dataset analysed needs to be sufficient, in particular to establish the baseline on the synonymous dataset. Here, despite a high replication (40 populations evolved in the exact same conditions), the total number of synonymous mutations that could be analysed was not very high and there was only one case of a gene with synonymous mutation in two independent populations. Second, although the models are able to identify factors affecting the mutation counts, the proportion of the variation explained is quite low. The consequence is that the models correctly predicts the mutation count distribution but the objective of predicting on which genes the response to selection will occur still seems quite far away.
The framework developed in this manuscript [1] clearly represents a very useful tool for the analysis of large “evolve and resequence” data sets and to gain a better understanding of the determinants of parallel evolution in general. The extension of its application to mutations others than SNPs would provide the possibility to get a more complete picture of the differences in contributions of mutation and selection intensity heterogeneities depending on the mutation types.

References

[1] Bailey SF, Guo Q and Bataillon T (2018) Identifying drivers of parallel evolution: A regression model approach. bioRxiv 118695, ver. 4 peer-reviewed by Peer Community In Evolutionary Biology. doi: 10.1101/118695

[2] Lang GI, Rice DP, Hickman, MJ, Sodergren E, Weinstock GM, Botstein D, and Desai MM (2013) Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature 500: 571–574. doi: 10.1038/nature12344

Identifying drivers of parallel evolution: A regression model approachSusan F Bailey, Qianyun Guo, Thomas Bataillon<p>This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (http://dx.doi.org/10.24072/pci.evolbiol.100045). Parallel evolution, defined as identical changes arising in independent populations, is often attributed...Experimental Evolution, Molecular EvolutionStephanie Bedhomme2017-03-22 14:54:48 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.

References

[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
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.
 

References

[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
31 Jul 2017
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Selection on morphological traits and fluctuating asymmetry by a fungal parasite in the yellow dung fly

Parasite-mediated selection promotes small body size in yellow dung flies

Recommended by based on reviews by Rodrigo Medel and 1 anonymous reviewer

Body size has long been considered as one of the most important organismic traits influencing demographical processes, population size, and evolution of life history strategies [1, 2]. While many studies have reported a selective advantage of large body size, the forces that determine small-sized organisms are less known, and reports of negative selection coefficients on body size are almost absent at present. This lack of knowledge is unfortunate as climate change and energy demands in stressful environments, among other factors, may produce new selection scenarios and unexpected selection surfaces [3]. In this manuscript, Blanckenhorn [4] reports on a potential explanation for the surprising 10% body size decrease observed in a Swiss population of yellow dung flies during 1993 - 2009. The author took advantage of a fungus outbreak in 2002 to assess the putative role of the fungus Entomopthora scatophagae, a specific parasite of adult yellow dung flies, as selective force acting upon host body size. His findings indicate that, as expected by sexual selection theory, large males experience a mating advantage. However, this positive sexual selection is opposed by a strong negative selection on male and female body size through the viability fitness component. This study provides the first evidence of parasite-mediated disadvantage of large adult body size in the field. While further experimental work is needed to elucidate the exact causes of body size reduction in the population, the author proposes a variation of the trade-off hypothesis raised by Rantala & Roff [5] that large-sized individuals face an immunity cost due to their high absolute energy demands in stressful environments.

References

[1] Peters RH. 1983. The ecological implications of body size. Cambridge University Press, Cambridge.

[2] Schmidt-Nielsen K. 1984. Scaling: why is animal size so important? Cambridge University Press, Cambridge.

[3] Ohlberger J. 2013. Climate warming and ectotherm body size: from individual physiology to community ecology. Functional Ecology 27: 991-1001. doi: 10.1111/1365-2435.12098

[4] Blanckenhorn WU. 2017. Selection on morphological traits and fluctuating asymmetry by a fungal parasite in the yellow dung fly. bioRxiv 136325, ver. 2 of 29th June 2017. doi: 10.1101/136325

[5] Rantala MJ & Roff DA. 2005. An analysis of trade-offs in immune function, body size and development time in the Mediterranean field cricket, Gryllus bimaculatus. Functional Ecology 19: 323-330. doi: 10.1111/j.1365-2435.2005.00979.x

Selection on morphological traits and fluctuating asymmetry by a fungal parasite in the yellow dung flyWolf U. BlanckenhornEvidence for selective disadvantages of large body size remains scarce in general. Previous phenomenological studies of the yellow dung fly *Scathophaga stercoraria* have demonstrated strong positive sexual and fecundity selection on male and fema...Behavior & Social Evolution, Evolutionary Ecology, Life History, Sexual SelectionRodrigo Medel Rodrigo Medel2017-05-10 11:16:26 View
05 Dec 2017
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Reconstruction of body mass evolution in the Cetartiodactyla and mammals using phylogenomic data

Predicting small ancestors using contemporary genomes of large mammals

Recommended by based on reviews by Bruce Rannala and 1 anonymous reviewer

Recent methodological developments and increased genome sequencing efforts have introduced the tantalizing possibility of inferring ancestral phenotypes using DNA from contemporary species. One intriguing application of this idea is to exploit the apparent correlation between substitution rates and body size to infer ancestral species' body sizes using the inferred patterns of substitution rate variation among species lineages based on genomes of extant species [1].
The recommended paper by Figuet et al. [2] examines the utility of such approaches by analyzing the Cetartiodactyla, a clade of large mammals that have mostly well resolved phylogenetic relationships and a reasonably good fossil record. This combination of genomic data and fossils allows a direct comparison between body size predictions obtained from the genomic data and empirical evidence from the fossil record. If predictions seem good in groups such as the Cetartiodactyla, where there is independent evidence from the fossil record, this would increase the credibility of predictions made for species with less abundant fossils.
Figuet et al. [2] analyze transcriptome data for 41 species and report a significant effect of body mass on overall substitution rate, synonymous vs. non-synonymous rates, and the dynamics of GC-content, thus allowing a prediction of small ancestral body size in this group despite the fact that the extant species that were analyzed are nearly all large.
A comparative method based solely on morphology and phylogenetic relationships would be very unlikely to make such a prediction. There are many sources of uncertainty in the variables and parameters associated with these types of approaches: phylogenetic uncertainty (topology and branch lengths), uncertainty about inferred substitution rates, and so on. Although the authors do not account for all these sources of uncertainty the fact that their predicted body sizes appear sensible is encouraging and undoubtedly the methods will become more statistically sophisticated over time.

References

[1] Romiguier J, Ranwez V, Douzery EJP and Galtier N. 2013. Genomic evidence for large, long-lived ancestors to placental mammals. Molecular Biology and Evolution 30: 5–13. doi: 10.1093/molbev/mss211

[2] Figuet E, Ballenghien M, Lartillot N and Galtier N. 2017. Reconstruction of body mass evolution in the Cetartiodactyla and mammals using phylogenomic data. bioRxiv, ver. 3 of 4th December 2017. 139147. doi: 10.1101/139147

Reconstruction of body mass evolution in the Cetartiodactyla and mammals using phylogenomic dataEmeric Figuet, Marion Ballenghien, Nicolas Lartillot, Nicolas Galtier<p>Reconstructing ancestral characters on a phylogeny is an arduous task because the observed states at the tips of the tree correspond to a single realization of the underlying evolutionary process. Recently, it was proposed that ancestral traits...Genome Evolution, Life History, Macroevolution, Molecular Evolution, Phylogenetics / PhylogenomicsBruce Rannala2017-05-18 15:28:58 View