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13 Dec 2016
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Addicted? Reduced host resistance in populations with defensive symbionts

Hooked on Wolbachia

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This very nice paper by Martinez et al. [1] provides further evidence, if further evidence was needed, of the extent to which heritable microorganisms run the evolutionary show.
Wolbachia is an ubiquitous endosymbiont of arthropods who has been recently shown to protect its hosts against viral infections. Here, Martinez et al. are able to show that this multifaceted heritable symbiont weakens selective pressures induced by viruses on host immune genes. In a series of very elegant experiments, Wolbachia-infected and Wolbachia-free populations of D. melanogaster were exposed to Drosophila C virus (a natural, and highly virulent Drosophila pathogen). At the end of a 9-generation artificial selection protocol with DCV, resistance against DCV increased in flies, both in the presence and absence of Wolbachia. Wolbachia-infected flies were still substantially more resistant to DCV viruses than their Wolbachia-free counterparts. Crucially, however, the frequency of the pastrel resistant allele (a key immune gene for DCV resistance) was significantly lower in the Wolbachia-infected lines. As a consequence, when the DCV-evolved lines were treated with antibiotics to cure them from the bacterial infection, the lines who had evolved with Wolbachia tended to be more susceptible to the virus than their uninfected counterparts.
In other words, infection by protective heritable symbionts can affect how selection acts on the host's nuclear-based resistance, effectively rendering it dependent on its symbiont for the fight against pathogens.
But the interest of these results may not be simply academic. The protective qualities of Wolbachia against a range of pathogens have opened up the exciting possibility of transferring these bacteria to mosquito vectors of key human diseases such as dengue or malaria. The long term evolutionary potential for these novel Wolbachia-host interactions has, however, been little explored. Either the Wolbachia, the pathogen or, as shown here, the host, could evolve in more or less predictable ways. There is, for example, evidence showing that in novel hosts Wolbachia evolves rapidly and tends to gradually lose its virulence. If the lost virulence was to result in a decrease in their pathogen defensive qualities, the mosquito, having lost the efficiency of its conventional immune defences, could end up being more vulnerable to infection than before the Wolbachia introduction. Martinez et al.'s paper is a nice example of how investigating the evolutionary potential of such Wolbachia-host-pathogen interactions can be hugely informative as to the long term prospects of these new control methods.

Reference

[1] Martinez J, Cogni R, Cao C, Smith S, Illingworth CJR & Jiggins FM. 2016. Addicted? Reduced host resistance in populations with defensive symbionts. Proceedings of the Royal Society of London B 283:20160778. doi: 10.1098/rspb.2016.0778

Addicted? Reduced host resistance in populations with defensive symbiontsMartinez J, Cogni R, Cao C, Smith S, Illingworth CJR & Jiggins FM<p>Heritable symbionts that protect their hosts from pathogens have been described in a wide range of insect species. By reducing the incidence or severity of infection, these symbionts have the potential to reduce the strength of selection on gen...Adaptation, Evolutionary Applications, Evolutionary Ecology, Experimental Evolution, Life HistoryAna Rivero2016-12-13 20:08:37 View
13 Nov 2017
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Epidemiological trade-off between intra- and interannual scales in the evolution of aggressiveness in a local plant pathogen population

The pace of pathogens’ adaptation to their host plants

Recommended by based on reviews by Benoit Moury and 1 anonymous reviewer

Because of their shorter generation times and larger census population sizes, pathogens are usually ahead in the evolutionary race with their hosts. The risks linked to pathogen adaptation are still exacerbated in agronomy, where plant and animal populations are not freely evolving but depend on breeders and growers, and are usually highly genetically homogeneous. As a consequence, the speed of pathogen adaptation is crucial for agriculture sustainability. Unraveling the time scale required for pathogens’ adaptation to their hosts would notably greatly improve our estimation of the risks of pathogen emergence, the efficiency of disease control strategies and the design of epidemiological surveillance schemes. However, the temporal scale of pathogen evolution has received much less attention than its spatial scale [1]. In their study of a wheat fungal disease, Suffert et al. [2] reached contrasting conclusions about the pathogen adaptation depending on the time scale (intra- or inter-annual) and on the host genotype (sympatric or allopatric) considered, questioning the experimental assessment of this important problem.

Suffert et al. [2] sampled two pairs of Zymoseptoria tritici (the causal agent of septoria leaf blotch) sub-populations in a bread wheat field plot, representing (i) isolates collected at the beginning or at the end of an epidemic in a single growing season (2009-2010 intra-annual sampling scale) and (ii) isolates collected from plant debris at the end of growing seasons in 2009 and in 2015 (inter-annual sampling scale). Then, they measured in controlled conditions two aggressiveness traits of the isolates of these four Z. tritici sub-populations, the latent period and the lesion size on leaves, on two wheat cultivars. One of the cultivars was considered as "sympatric" because it was at the source of the studied isolates and was predominant in the growing area before the experiment, whereas the other cultivar was considered as "allopatric" since it replaced the previous one and became predominant in the growing area during the sampling period.

On the sympatric host, at the intra-annual scale, they observed a marginally-significant decrease in latent period and a significant decrease of the between-isolate variance for this trait, which are consistent with a selection of pathogen variants with an enhanced aggressiveness. In contrast, at the inter-annual scale, no difference in the mean or variance of aggressiveness trait values was observed on the sympatric host, suggesting a lack of pathogen adaptation. They interpreted the contrast between observations at the two time scales as the consequence of a trade-off for the pathogen between a gain of aggressiveness after several generations of asexual reproduction at the intra-annual scale and a decrease of the probability to reproduce sexually and to be transmitted from one growing season to the next. Indeed, at the end of the growing season, the most aggressive isolates are located on the upper leaves of plants, where the pathogen density and hence probably also the probability to reproduce sexually, is lower. On the allopatric host, the conclusion about the pathogen stability at the inter-annual scale was somewhat different, since a significant increase in the mean lesion size was observed (isolates corresponding to the intra-annual scale were not checked on the allopatric host). This shows the possibility for the pathogen to evolve at the inter-annual scale, for a given aggressiveness trait and on a given host.

In conclusion, Suffert et al.’s [2] study emphasizes the importance of the experimental design in terms of sampling time scale and host genotype choice to analyze the pathogen adaptation to its host plants. It provides also an interesting scenario, at the crossroad of the pathogen’s reproduction regime, niche partitioning and epidemiological processes, to interpret these contrasted results. Pathogen adaptation to plant cultivars with major-effect resistance genes is usually fast, including in the wheat-Z. tritici system [3]. Therefore, this study will be of great help for future studies on pathogen adaptation to plant partial resistance genes and on strategies of deployment of such resistance at the landscape scale.

References
[1] Penczykowski RM, Laine A-L and Koskella B. 2016. Understanding the ecology and evolution of host–parasite interactions across scales. Evolutionary Applications, 9: 37–52. doi: 10.1111/eva.12294

[2] Suffert F, Goyeau H, Sache I, Carpentier F, Gelisse S, Morais D and Delestre G. 2017. Epidemiological trade-off between intra- and interannual scales in the evolution of aggressiveness in a local plant pathogen population. bioRxiv, 151068, ver. 3 of 12th November 2017. doi: 10.1101/151068

[3] Brown JKM, Chartrain L, Lasserre-Zuber P and Saintenac C. 2015. Genetics of resistance to Zymoseptoria tritici and applications to wheat breeding. Fungal Genetics and Biology, 79: 33–41. doi: 10.1016/j.fgb.2015.04.017

Epidemiological trade-off between intra- and interannual scales in the evolution of aggressiveness in a local plant pathogen populationFrederic Suffert, Henriette Goyeau, Ivan Sache, Florence Carpentier, Sandrine Gelisse, David Morais, Ghislain DelestreThe efficiency of plant resistance to fungal pathogen populations is expected to decrease over time, due to its evolution with an increase in the frequency of virulent or highly aggressive strains. This dynamics may differ depending on the scale i...Adaptation, Evolutionary Applications, Evolutionary EpidemiologyBenoit Moury2017-06-23 21:04:54 View
02 May 2023
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Durable resistance or efficient disease control? Adult Plant Resistance (APR) at the heart of the dilemma

Plant resistance to pathogens: just you wait?

Recommended by based on reviews by Jean-Paul Soularue and 1 anonymous reviewer

In this preprint, Rimbaud et al. (2023) examine whether Adult Plant Resistance (APR), where plants delay their response to pathogens, is a viable alternative when the solution to evolve complete resistance from the seedling stage exists. At first glance, delaying resistance seems like a counter-intuitive strategy, unless it can result in a weaker selection of the pathogen, and therefore slow down its adaption to plant resistance.

The approach of Rimbaud et al. is to incorporate as much of the mechanisms as possible into a model. By accounting for explicit spatio-temporal dynamics, stochasticity, and the coupling between demography and population genetics, to simulate an agricultural landscape, they reach a nuanced conclusion.

Weaker and delayed activation of genes that confer APR does indeed reduce the selection pressure acting on the pathogen, at the cost of overall less effective protection. The alternative strategy of rapid or complete activation of these genes, although it results in better results in defending against the pathogen, is at risk of being overcome because it introduces a stronger selection pressure.

One important feature of this work is that it accounts for agricultural practices. The landscape that is simulated can account for monoculture, mosaic cultures, mixed cultures, and rotations of crops (with different strategies for resistance). This introduces an interesting element to the conclusion: that human practices will have an impact on the selection pressures acting within the system.

Perhaps the most striking result is that, for the plants, it might be more beneficial to bear the cost of a wild-type pathogen that can benefit from delayed activation of resistance, and therefore exclude the more virulent strains by simply being there first, and essentially buying the plant some time before it activates its resistance more completely. When the landscape is aggregated, even wild-type pathogens can cause severe epidemics; increasing fragmentation, because it enables connectivity between patches of plants with different strategies, allows pathogens to move across cultivars, and reduces the epidemic risk on susceptible plants.

These results should encourage scaling up the perspective on APR, and indeed Rimbaud et al. adopt a landscape-scale perspective, to show that APR genes and genes conferring more complete resistance early on can have synergistic effects. This is, again, both an interesting result for evolutionary biologists, but also a useful way to prioritize different crop management strategies over large spatial scales.

References

Rimbaud, Loup, et al. Durable Resistance or Efficient Disease Control? Adult Plant Resistance (APR) at the Heart of the Dilemma. 2023. bioRxiv, ver. 2 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.08.30.505787

Durable resistance or efficient disease control? Adult Plant Resistance (APR) at the heart of the dilemmaLoup Rimbaud, Julien Papaïx, Jean-François Rey, Benoît Moury, Luke G. Barrett, Peter H. Thrall<p style="text-align: justify;">Adult plant resistance (APR) is an incomplete and delayed protection of plants against pathogens. At first glance, such resistance should be less efficient than classical major-effect resistance genes, which confer ...Adaptation, Evolutionary Applications, Evolutionary EpidemiologyTimothée Poisot2022-09-02 16:36:32 View
16 Dec 2016
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Spatiotemporal microbial evolution on antibiotic landscapes

A poster child for experimental evolution

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Evolution is usually studied via two distinct approaches: by inferring evolutionary processes from relatedness patterns among living species or by observing evolution in action in the laboratory or field. A recent study by Baym and colleagues in Science [1] has now combined these approaches by taking advantage of the pattern left behind by spatially evolving bacterial populations.

Evolution is often considered too slow to see, and can only be inferred by studying patterns of relatedness using phylogenetic trees. Increasingly, however, researchers are moving nature into the lab and watching as evolution unfolds under their noses. The field of experimental evolution follows evolutionary change in the laboratory over 10s to 1000s of generations, yielding insights into bacterial, viral, plant, or fly evolution (among many other species) that are simply not possible in the field. Yet, as powerful as experimental evolution is, it lacks a posterchild. There is no Galapagos finch radiation, nor a stunning series of cichlids to showcase to our students to pique their interests. Let’s face it, E. coli is no stickleback! And while practitioners of experimental evolution can explain the virtues of examining 60,000 generations of bacterial evolution in action, appreciating this nevertheless requires a level of insight and imagination that often eludes students, who need to see “it” to get it.

Enter MEGA, an idea and a film that could become the new face of experimental evolution. It replaces big numbers of generations or images of scientists, with an actual picture of the scientific result. MEGA, or Microbial Evolution and Growth Arena, is essentially an enormous petri dish and is the brainchild of Michael Baym, Tami Leiberman and their colleagues in Roy Kishony’s lab at Technion Israel Institute of Technology and Harvard Medical School. The idea of MEGA is to allow bacteria to swim over a spatially defined landscape while adapting to the local conditions, in this case antibiotics. When bacteria are inoculated onto one end of the plate they consume resources while swarming forward from the plate edge. In a few days, the bacteria grow into an area with antibiotics to which they are susceptible. This stops growth until a mutation arises that permits the bacteria to jump this hurdle, after which growth proceeds until the next hurdle of a 10-fold higher antibiotic concentration, and so on. By this simple approach, Baym et al. [1] evolved E. coli that were nearly 105-fold more resistant to two different antibiotics in just over 10 days. In addition, they identified the mutations that were required for these changes, showed that mutations conferring smaller benefits were required before bacteria could evolve maximal resistance, observed changes to the mutation rate, and demonstrated the importance of spatial structure in constraining adaptation.

For one thing, the rate of resistance evolution is impressive, and also quite scary given the mounting threat of antibiotic-resistant pathogens. However, MEGA also offers a uniquely visual insight into evolutionary change. By taking successive images of the MEGA plate, the group was able to watch the bacteria move, get trapped because of their susceptibility to the antibiotic, and then get past these traps as new mutations emerged that increased resistance. Each transition showcases evolution in real time. In addition, by leaving a spatial pattern of evolutionary steps behind, the MEGA plate offers unique opportunities to thoroughly investigate these steps when the experiment is finished. For instance, subsequent steps in mutational pathways can be characterized, but also their effects on fitness can be quantified in situ by measuring changes in survival and reproduction. This new method is undoubtedly a boon to the field of experimental evolution and offers endless opportunities for experimental elaboration. Perhaps of equal importance, MEGA is a tool that is portable to the classroom and to the public at large. Don’t believe in evolution? Watch this. You only have time for a short internship or lab practical? No problem. Don’t worry much about antibiotic resistance? Check this out. Like the best experimental tools, MEGA is simple but allows for complicated insights. And even if it is less charismatic than a finch, it still allows for the kinds of “gee-whiz” insights that will get students hooked on evolutionary biology.

Reference

[1] Baym M, Lieberman TD, Kelsic ED, Chait R, Gross R, Yelin I, Kishony R. 2016. Spatiotemporal microbial evolution on antibiotic landscapes. Science 353:1147-1151. doi: 10.1126/science.aag0822

Spatiotemporal microbial evolution on antibiotic landscapesBaym M, Lieberman TD, Kelsic ED, Chait R, Gross R, Yelin I, Kishony R<p>A key aspect of bacterial survival is the ability to evolve while migrating across spatially varying environmental challenges. Laboratory experiments, however, often study evolution in well-mixed systems. Here, we introduce an experimental devi...Adaptation, Evolutionary Applications, Experimental EvolutionDaniel Rozen2016-12-14 14:26:06 View
05 Nov 2020
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A genomic amplification affecting a carboxylesterase gene cluster confers organophosphate resistance in the mosquito Aedes aegypti: from genomic characterization to high-throughput field detection

Identification of a gene cluster amplification associated with organophosphate insecticide resistance: from the diversity of the resistance allele complex to an efficient field detection assay

Recommended by based on reviews by Diego Ayala and 2 anonymous reviewers

The emergence and spread of insecticide resistance compromises the efficiency of insecticides as prevention tool against the transmission of insect-transmitted diseases (Moyes et al. 2017). In this context, the understanding of the genetic mechanisms of resistance and the way resistant alleles spread in insect populations is necessary and important to envision resistance management policies. A common and important mechanism of insecticide resistance is gene amplification and in particular amplification of insecticide detoxification genes, which leads to the overexpression of these genes (Bass & Field, 2011). Cattel and coauthors (2020) adopt a combination of experimental approaches to study the role of gene amplification in resistance to organophosphate insecticides in the mosquito Aedes aegypti and its occurrence in populations of South East Asia and to develop a molecular test to track resistance alleles.
Their first approach consists in performing an artificial selection on laboratory Ae. Aegypti populations started with individuals collected in Laos. In the selected population, an initial 90% mortality by adult exposure to the organophosphate insecticide malathion is imposed. This population shows a steep increase in resistance to malathion and other organophosphate insecticides, which is absent in the paired control population. The transcriptomic patterns of the control and the evolved populations as well as of a reference sensitive population reveals, among other differences, the over-expression of five carboxy/choline esterase (CCE) genes in the insecticide selected population. These five genes happen to be clustered in the Ae. aegypti genome and whole genome sequencing of a highly resistant population combined to qPCR test on genomic DNA showed that the overexpression of these genes is due to gene amplification. Although it would have been more elegant to have replicate selected and control populations and to perform the transcriptomic and the genomic analyses directly on the experimental populations, the authors gather a set of experimental evidence which combined to previous knowledge on the function of the amplified and over-expressed genes and on their implication in organophosphate insecticide resistance in other species allow to discard the possibility that this gene amplification spread by drift in the selected population.
In a second part of the paper, copy number variation for CCE genes is checked in field sample populations. This test reveals the presence of resistance alleles in half of the fourteen South East Asia populations sampled. Very interestingly, it also reveals a high level of complexity and diversity among the resistance alleles: it shows first the existence, both in the experimental and the field populations, of at least two amplified alleles (differing by the number of genes amplified) and second a high variation in the copy number of amplified genes. This indicates that gene amplification as a molecular resistance mechanism has actually lead to a high diversity of resistance alleles. These alleles are likely to differ both by the level of resistance conferred and the fitness cost imposed in the absence of the insecticide and these two values are affecting the evolution of their frequency in the field and ultimately the spread of resistance.
The last part of the paper is devoted to the development of a high-throughput Taqman assay which allows to determine rapidly the copy number of one of the esterase genes amplified in the resistance alleles described earlier. This assay is nicely validated and will definitely be a useful tool to determine the occurrence of these resistance alleles in field population. The fact that it gives access to the copy number will also allow to follow its copy number across time and get insight into the complexity of resistance evolution by gene amplification.
To sum up, this paper studies the implication of carboxy/choline esterase genes amplification in organophosphate resistance evolution in Ae. aegypti, reveals the diversity among individuals and populations of this resistance mechanism, because of variation both in the identity of the genes amplified and in their copy number and sets up a fast and efficient tool to detect and follow the spread of these resistant alleles in the field. Additionally, the different experimental approaches adopted have generated genomic and transcriptomic data, of which only the part related to CCE gene amplification has been exploited. These data are very likely to reveal other genomic and expression determinants of resistance that will give access to an extra degree of complexity in organophosphate insecticide resistance determinism and evolution.

References

Bass C, Field LM (2011) Gene amplification and insecticide resistance. Pest Management Science, 67, 886–890. https://doi.org/10.1002/ps.2189
Cattel J, Haberkorn C, Laporte F, Gaude T, Cumer T, Renaud J, Sutherland IW, Hertz JC, Bonneville J-M, Arnaud V, Nous C, Fustec B, Boyer S, Marcombe S, David J-P (2020) A genomic amplification affecting a carboxylesterase gene cluster confers organophosphate resistance in the mosquito Aedes aegypti: from genomic characterization to high-throughput field detection. bioRxiv, 2020.06.08.139741, ver. 4 peer-reviewed and recommended by PCI Evolutionary Biology. https://doi.org/10.1101/2020.06.08.139741
Moyes CL, Vontas J, Martins AJ, Ng LC, Koou SY, Dusfour I, Raghavendra K, Pinto J, Corbel V, David J-P, Weetman D (2017) Contemporary status of insecticide resistance in the major Aedes vectors of arboviruses infecting humans. PLOS Neglected Tropical Diseases, 11, e0005625. https://doi.org/10.1371/journal.pntd.0005625

A genomic amplification affecting a carboxylesterase gene cluster confers organophosphate resistance in the mosquito Aedes aegypti: from genomic characterization to high-throughput field detectionJulien Cattel, Chloé Haberkorn, Fréderic Laporte, Thierry Gaude, Tristan Cumer, Julien Renaud, Ian W. Sutherland, Jeffrey C. Hertz, Jean-Marc Bonneville, Victor Arnaud, Camille Noûs, Bénédicte Fustec, Sébastien Boyer, Sébastien Marcombe, Jean-Phil...<p>By altering gene expression and creating paralogs, genomic amplifications represent a key component of short-term adaptive processes. In insects, the use of insecticides can select gene amplifications causing an increased expression of detoxifi...Adaptation, Evolutionary Applications, Experimental Evolution, Genome Evolution, Molecular EvolutionStephanie Bedhomme2020-06-09 13:27:18 View
23 Apr 2020
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How do invasion syndromes evolve? An experimental evolution approach using the ladybird Harmonia axyridis

Selection on a single trait does not recapitulate the evolution of life-history traits seen during an invasion

Recommended by and based on reviews by 2 anonymous reviewers

Biological invasions are natural experiments, and often show that evolution can affect dynamics in important ways [1-3]. While we often think of invasions as a conservation problem stemming from anthropogenic introductions [4,5], biological invasions are much more commonplace than this, including phenomena as diverse as natural range shifts, the spread of novel pathogens, and the growth of tumors. A major question across all these settings is which set of traits determine the ability of a population to invade new space [6,7]. Traits such as: increased growth or reproductive rate, dispersal ability and ability to defend from predation often show large evolutionary shifts across invasion history [1,6,8]. Are such multi-trait shifts driven by selection on multiple traits, or a correlated response by multiple traits to selection on one? Resolving this question is important for both theoretical and practical reasons [9,10]. But despite the importance of this issue, it is not easy to perform the necessary manipulative experiments [9].
Foucaud et al. [11] tackled this issue by performing experimental evolution on source populations of the invasive ladybug Harmonia axyridis. The authors tested if selection on a single trait could generate correlated responses in other life history traits. Specifically, they used experimental evolution to impose divergent selection on female mass, and reproductive timing. After ten generations, they found that selection for weight did not affect almost any other life history trait. However, nine generations of selection for faster reproduction led to correlated phenotypic changes in developmental, reproduction and survival rate of populations, although not always in the direction we might have expected. Despite this correlated response, none of their selected lines were able to fully recapitulate the trait shifts seen in natural invasions of this species. This implies that selection during natural invasions is operating on multiple traits; a finding in agreement with our growing understanding of how selection acts during introduction and invasion [12,13].
Populations undergoing a colonization process may also be subject to a multitude of different selective pressures [14,15]. The authors expanded their work in this direction by testing whether food availability alters the observed correlations between life history traits. The pervasiveness of genotype by environment interactions observed also points to a role for multiple selective pressures in shaping the suite of life-history shifts observed in wild ladybug populations. The work from Foucaud and colleagues [11] adds to a small but growing list of important studies that use experimental evolution to investigate how life-history traits evolve, and how they evolve during invasions in particular.

References

[1] Sakai, A.K., Allendorf, F.W., Holt, J.S. et al. (2001). The population biology of invasive species. Annual review of ecology and systematics, 32(1), 305-332. doi: 10.1146/annurev.ecolsys.32.081501.114037
[2] Hairston Jr, N. G., Ellner, S. P., Geber, M. A., Yoshida, T. and Fox, J. A. (2005). Rapid evolution and the convergence of ecological and evolutionary time. Ecology letters, 8(10), 1114-1127. doi: 10.1111/j.1461-0248.2005.00812.x
[3] Chuang, A. and Peterson, C. R. (2016). Expanding population edges: theories, traits, and trade‐offs. Global change biology, 22(2), 494-512. doi: 10.1111/gcb.13107
[4] Whitney, K. D. and Gabler, C. A. (2008). Rapid evolution in introduced species,‘invasive traits’ and recipient communities: challenges for predicting invasive potential. Diversity and Distributions, 14(4), 569-580. doi: 10.1111/j.1472-4642.2008.00473.x
[5] Catullo, R. A., Llewelyn, J., Phillips, B. L. and Moritz, C. C. (2019). The Potential for Rapid Evolution under Anthropogenic Climate Change. Current Biology, 29(19), R996-R1007. doi: 10.1016/j.cub.2019.08.028
[6] Suarez, A. V. and Tsutsui, N. D. (2008). The evolutionary consequences of biological invasions. Molecular Ecology, 17(1), 351-360. doi: 10.1111/j.1365-294X.2007.03456.x
[7] Deforet, M., Carmona-Fontaine, C., Korolev, K. S. and Xavier, J. B. (2019). Evolution at the edge of expanding populations. The American Naturalist, 194(3), 291-305. doi: 10.1086/704594
[8] Phillips, B. L., Brown, G. P., and Shine, R. (2010). Life‐history evolution in range‐shifting populations. Ecology, 91(6), 1617-1627. doi: 10.1890/09-0910.1
[9] Colautti, R. I. and Lau, J. A. (2015). Contemporary evolution during invasion: evidence for differentiation, natural selection, and local adaptation. Molecular ecology, 24(9), 1999-2017. doi: 10.1111/mec.13162
[10] Szűcs, M., Melbourne, B. A., Tuff, T., Weiss‐Lehman, C. and Hufbauer, R. A. (2017). Genetic and demographic founder effects have long‐term fitness consequences for colonising populations. Ecology Letters, 20(4), 436-444. doi: 10.1111/ele.12743
[11] Foucaud, J., Hufbauer, R. A., Ravigné, V., Olazcuaga, L., Loiseau, A., Ausset, A., Wang, S., Zang, L.-S., Lemenager, N., Tayeh, A., Weyna, A., Gneux, P., Bonnet, E., Dreuilhe, V., Poutout, B., Estoup, A. and Facon, B. (2020). How do invasion syndromes evolve? An experimental evolution approach using the ladybird Harmonia axyridis. bioRxiv, 849968 ver. 4 peer-reviewed and recommended by PCI Evolutionary Biology. doi: 10.1101/849968
[12] Simons, A. M. (2003). Invasive aliens and sampling bias. Ecology Letters, 6(4), 278-280. doi: 10.1046/j.1461-0248.2003.00430.x
[13] Phillips, B. L. and Perkins, T. A. (2019). Spatial sorting as the spatial analogue of natural selection. Theoretical Ecology, 12(2), 155-163. doi: 10.1007/s12080-019-0412-9
[14] Lavergne, S. and Molofsky, J. (2007). Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proceedings of the National Academy of Sciences, 104(10), 3883-3888. doi: 10.1073/pnas.0607324104
[15] Moran, E. V. and Alexander, J. M. (2014). Evolutionary responses to global change: lessons from invasive species. Ecology Letters, 17(5), 637-649. doi: 10.1111/ele.12262

How do invasion syndromes evolve? An experimental evolution approach using the ladybird Harmonia axyridisJulien Foucaud, Ruth A. Hufbauer, Virginie Ravigné, Laure Olazcuaga, Anne Loiseau, Aurelien Ausset, Su Wang, Lian-Sheng Zang, Nicolas Lemenager, Ashraf Tayeh, Arthur Weyna, Pauline Gneux, Elise Bonnet, Vincent Dreuilhe, Bastien Poutout, Arnaud Est...<p>Experiments comparing native to introduced populations or distinct introduced populations to each other show that phenotypic evolution is common and often involves a suit of interacting phenotypic traits. We define such sets of traits that evol...Adaptation, Evolutionary Applications, Experimental Evolution, Life History, Quantitative GeneticsInês Fragata2019-11-29 07:07:00 View
18 Nov 2024
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A genomic duplication spanning multiple P450s contributes to insecticide resistance in the dengue mosquito Aedes aegypti

A duplication driving metabolic insecticide resistance in Aedes aegypti

Recommended by ORCID_LOGO based on reviews by Diego Ayala and 1 anonymous reviewer

Insecticide resistance in mosquitoes represents a notable challenge to public health efforts aimed at controlling vector-borne diseases. Among mosquito species, Aedes aegypti is particularly significant due to its extensive geographic spread and its ability to transmit arboviruses causing diseases such as dengue, yellow fever, Zika, and chikungunya (Brown et al., 2014). Insecticide resistance typically develops through two main mechanisms: target-site mutations, which affect the insecticide's interaction with its target, and metabolic resistance, in which insecticide detoxification is enhanced in mosquitoes. While target-site mutations are well characterized, the mechanisms underlying metabolic resistance are understudied. 

The study by Bacot and colleagues (2024) contributes to our understanding of the genetic and evolutionary mechanisms driving insecticide resistance, focusing on a case of metabolic resistance in Aedes aegypti from French Guiana. Following the recent identification of a copy number variant region on chromosome 1, potentially linked to overexpression of detoxification enzymes (Cattel et al., 2020), this study explores the region’s genomic architecture, its likely origin and provides compelling evidence for its role in insecticide resistance.

Through RNA sequencing and whole-genome pool sequencing, the authors reveal that this 220 kilobase duplication increases the expression level of several clustered P450 genes. Cytochrome P450s are known to play a role in breaking down pyrethroids like deltamethrin, a commonly used insecticide. The role of P450 enzymes in detoxification was demonstrated by treating mosquitoes with piperonyl butoxide, a P450 enzyme inhibitor, and observing reduction in deltamethrin resistance, further confirmed by RNA interference experiments. Despite the clear advantages of this genomic duplication in conferring resistance, the study also uncovers a fitness cost associated with carrying the duplication. Through experimental evolution, the authors find that mosquitoes with the duplication experience reduced fitness in the absence of insecticide pressure. Given the regions structural complexity, the authors could not completely disassociate the effect of the duplicated region and that of a target-site mutation. However, they developed an assay that can accurately track the presence of this resistance allele in mosquito populations. 

Altogether, the study by Bacot et al. (2024) highlights the challenges of characterizing the phenotypic effect of copy number variant regions in complex genomes, such as that of Aedes aegypti. It emphasizes the need for further studies on the origin and spread of this duplication to better understand how similar resistance mechanisms might evolve and disseminate. Overall, the completeness and coherence of the narrative, the detailed and thorough analysis, and the insightful discussion, make this work not only a significant contribution to the field of insecticide resistance but an interesting read for the general evolutionary biology community.   

References

Brown, J. E., Evans, B. R., Zheng, W., Obas, V., Barrera-Martinez, L., Egizi, A., Zhao, H., Caccone, A., & Powell, J. R. (2014). Human impacts have shaped historical and recent evolution in Aedes aegypti, the dengue and yellow fever mosquito. Evolution, 68(2), 514–525. https://doi.org/10.1111/evo.12281

Cattel, J., Faucon, F., Le Péron, B., Sherpa, S., Monchal, M., Grillet, L., Gaude, T., Laporte, F., Dusfour, I., Reynaud, S., & David, J. P. (2019). Combining genetic crosses and pool targeted DNA-seq for untangling genomic variations associated with resistance to multiple insecticides in the mosquito Aedes aegypti. Evolutionary applications, 13(2), 303–317. https://doi.org/10.1111/eva.12867

Tiphaine Bacot, Chloe Haberkorn, Joseph Guilliet, Julien Cattel, Mary Kefi, Louis Nadalin, Jonathan Filee, Frederic Boyer, Thierry Gaude, Frederic Laporte, Jordan Tutagata, John Vontas, Isabelle Dusfour, Jean-Marc Bonneville, Jean-Philippe David (2024) A genomic duplication spanning multiple P450s contributes to insecticide resistance in the dengue mosquito Aedes aegypti. bioRxiv, ver.5 peer-reviewed and recommended by PCI Evol Biol https://doi.org/10.1101/2024.04.03.587871

A genomic duplication spanning multiple P450s contributes to insecticide resistance in the dengue mosquito *Aedes aegypti*Tiphaine Bacot, Chloe Haberkorn, Joseph Guilliet, Julien Cattel, Mary Kefi, Louis Nadalin, Jonathan Filee, Frederic Boyer, Thierry Gaude, Frederic Laporte, Jordan Tutagata, John Vontas, Isabelle Dusfour, Jean-Marc Bonneville, Jean-Philippe David<p>Resistance of mosquitoes to insecticides is one example of rapid adaptation to anthropogenic selection pressures having a strong impact on human health and activities. Target-site modification and increased insecticide detoxification are the tw...Adaptation, Evolutionary Applications, Expression Studies, Genotype-PhenotypeDiego A. Hartasánchez2024-04-10 11:36:06 View
24 Oct 2024
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Cryptic species and hybridisation in corals: challenges and opportunities for conservation and restoration

How common cryptic coral diversity can blur biodiversity metrics and challenge management

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

Biological conservation aims at protecting the genetic diversity generated by evolutionary processes over the course of life's history on earth (Allendorf and Luikart 2007), and to be effective, it requires that its fundamental units (among which populations and species) be delimited as precisely as possible. This exercise is particularly important for corals because hybridisation and introgression have played a fundamental role in shaping their contemporary diversity (eg Veron 1995). 

In their review paper, Riginos et al (2024) show that 68% of nominal taxa investigated for genomic population structure bear the molecular signature of partial reproductive isolation, and can be considered as cryptic genetic groups. Another review study (published a day before the preprint of Riginos et al), converges in the finding that cryptic diversity is rampant in nominal coral species (Grupstra et al 2024). This result has strong bearing on the study of coral biology; as Riginos et al state, "any coral investigation that does not genotype the corals under study risks treating a heterogeneous mix of partially reproductively isolated taxa as a single species." The stakes are therefore high, given the ecological importance of corals and the ecosystem services they provide. 

While Grupstra et al (2024) discusses the impact of cryptic coral diversity in the context of functional differences in thermal adaptation and the processes that lead to cryptic lineages, Riginos et al (2024) provide a quantitative review of cryptic lineages within nominal species, providing reproducible criteria for delineation, details the importance of detecting hybrids, summarises how biodiversity metrics and conservation efforts can be biased by unrecognised cryptic lineages, offer recommendations on how to recognise and deal with cryptic diversity, and discuss how corals can be regarded as highly valuable model systems to study adaptation and speciation. The study of Riginos et al (2024) is therefore a must-read to all coral biologists, especially those involved in biological conservation.

References

Fred W. Allendorf  and Gordon Luikart (2007) Conservation and Genetics of Populations. Blackwell Publishing, Malden MA, USA.

Carsten G. B. Grupstra, Matías Gómez-Corrales, James E. Fifer, Hannah E. Aichelman, Kirstin S. Meyer-Kaiser, Carlos Prada, Sarah W. Davies (2024) Integrating cryptic diversity into coral evolution, symbiosis and conservation. Nat Ecol Evol 8, 622–636 (2024). https://doi.org/10.1038/s41559-023-02319-y

Cynthia Riginos, Iva Popovic, Zoe Meziere, Vhon Garcia, Ilha Byrne, Samantha Howitt, Hisatake Ishida, Kevin Bairos-Novak, Adriana Humanes, Hugo Scharfenstein, Thomas Richards, Ethan Briggs, Vanessa Clark, Chuan Lei, Mariam Khan, Katharine Prata (2024) Cryptic species and hybridisation in corals: challenges and opportunities for conservation and restoration. EcoEvoRxiv, ver.2 peer-reviewed and recommended by PCI Evol Biol https://doi.org/10.32942/X2502X

J. E. N. Veron (1995) Corals in Space and Time: The Biogeography and Evolution of the Scleractinia.  Cornell University Press

Cryptic species and hybridisation in corals: challenges and opportunities for conservation and restorationCynthia Riginos, Iva Popovic, Zoe Meziere, Vhon Garcia, Ilha Byrne, Samantha Howitt, Hisatake Ishida, Kevin Bairos-Novak, Adriana Humanes, Hugo Scharfenstein, Thomas Richards, Ethan Briggs, Vanessa Clark, Chuan Lei, Mariam Khan, Katharine Prata<p style="text-align: justify;">The conservation and management of coral reef ecosystems will benefit from accurate assessments of reef-building coral species diversity. However, the true diversity of corals may be obfuscated by cryptic yet geneti...Adaptation, Evolutionary Applications, Hybridization / Introgression, Population Genetics / Genomics, SpeciationEric Pante2024-02-15 10:29:46 View
05 Apr 2024
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Does the seed fall far from the tree? Weak fine scale genetic structure in a continuous Scots pine population

Weak spatial genetic structure in a large continuous Scots pine population – implications for conservation and breeding

Recommended by ORCID_LOGO based on reviews by Joachim Mergeay, Jean-Baptiste Ledoux and Roberta Loh

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

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

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

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

References

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

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

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

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

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

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

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

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

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

Does the seed fall far from the tree? Weak fine scale genetic structure in a continuous Scots pine populationAlina K. Niskanen, Sonja T. Kujala, Katri Kärkkäinen, Outi Savolainen, Tanja Pyhäjärvi<p>Knowledge of fine-scale spatial genetic structure, i.e., the distribution of genetic diversity at short distances, is important in evolutionary research and in practical applications such as conservation and breeding programs. In trees, related...Adaptation, Evolutionary Applications, Population Genetics / GenomicsMyriam Heuertz Joachim Mergeay2023-06-27 21:57:28 View
05 May 2020
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Meta-population structure and the evolutionary transition to multicellularity

The ecology of evolutionary transitions to multicellularity

Recommended by based on reviews by 2 anonymous reviewers

The evolutionary transition to multicellular life from free-living, single-celled ancestors has occurred independently in multiple lineages [1-5]. This evolutionary transition to cooperative group living can be difficult to explain given the fitness advantages enjoyed by the non-cooperative, single-celled organisms that still numerically dominate life on earth [1,6,7]. Although several hypotheses have been proposed to explain the transition to multicellularity, a common theme is the abatement of the efficacy of natural selection among the single cells during the free-living stage and the promotion of the efficacy of selection among groups of cells during the cooperative stage, an argument reminiscent of those from George Williams’ seminal book [8,9]. The evolution of life cycles appears to be a key step in the transition to multicellularity as it can align fitness advantages of the single-celled 'reproductive' stage with that of the cooperative 'organismal' stage [9-12]. That is, the evolution of life cycles allows natural selection to operate over timescales longer than that of the doubling time of the free-living cells [13]. Despite the importance of this issue, identifying the range of ecological conditions that reduce the importance of natural selection at the single-celled, free-living stage and increase the importance of selection among groups of cooperating cells has not been addressed empirically.
Rose et al [14] addressed this issue in a series of real time evolution experiments with bacteria in which they varied the intensity of between-group versus individual-level selection. Central to the experiment is an ecological scaffold that requires lineages to switch between free-living (reproductive) and group-living (organismal) life-stages. One ecological scenario severely limited natural selection at the single-celled, free-living stage by maintaining separation among the reproductive propagules originating from different organisms (groups of cells derived from a single ancestral cell). A second ecological scenario mixed the reproductive propagules from different organisms, leading to severe competition between single cells derived from both the same and other 'organisms'. These ecological scenarios lead to very different evolutionary outcomes. Limiting competition, and thus natural selection, at the reproductive propagule stage promoted traits that favored organismal fitness at the expense of cell division, while competition among single-cells favored traits that promote cell-level traits at the expense of group-level traits. The authors investigate a range of measures of cell and group-level performance in order to understand the mechanisms favoring organismal versus single-cell fitness. Importantly, an evolutionary trade-off between traits promoting organismal fitness and single-cell fitness appears to constrain maximizing fitness of both phases, especially when strong natural selection acts on the single-cell stage.
This article is incredibly thorough and utilizes multiple experiments and levels of argument in order to support the conclusions. The authors include considerable discussion of broader topics surrounding the immediate hypotheses throughout the article, which add both clarity and complexity. The complexity of the experiments, results, and the topic itself lead to a thought-heavy article in a throwback to the monographs of old; expect to read each section multiple times.

References

[1] Maynard Smith, J. and Szathmáry, E. (1995). The Major Transitions in Evolution. Oxford, UK: Freeman. p 346.
[2] Bonner, J. T. (1998). The origins of multicellularity. Integrative Biology: Issues, News, and Reviews: Published in Association with The Society for Integrative and Comparative Biology, 1(1), 27-36. doi: 10.1002/(SICI)1520-6602(1998)1:1<27::AID-INBI4>3.0.CO;2-6
[3] Kaiser, D. (2001). Building a multicellular organism. Annual review of genetics, 35(1), 103-123. doi: 10.1146/annurev.genet.35.102401.090145
[4] Medina, M., Collins, A. G., Taylor, J. W., Valentine, J. W., Lipps, J. H., Amaral-Zettler, L., and Sogin, M. L. (2003). Phylogeny of Opisthokonta and the evolution of multicellularity and complexity in Fungi and Metazoa. International Journal of Astrobiology, 2(3), 203-211. doi: 10.1017/S1473550403001551
[5] King, N. (2004). The unicellular ancestry of animal development. Developmental cell, 7(3), 313-325. doi: 10.1016/j.devcel.2004.08.010
[6] Michod R. E. (1999). Darwinian Dynamics. Evolutionary Transitions in Fitness and Individuality. Princeton, NJ: Princeton Univ. Press. p 262.
[7] Lynch, M. (2007). The frailty of adaptive hypotheses for the origins of organismal complexity. Proceedings of the National Academy of Sciences, 104(suppl 1), 8597-8604. doi: 10.1073/pnas.0702207104
[8] Williams, G. C. (1996). Adaptation and Natural Selection, Reprint edition. Princeton, NJ: Princeton Univ. Press.
[9] Grosberg, R. K., and Strathmann, R. R. (2007). The evolution of multicellularity: a minor major transition?. Annu. Rev. Ecol. Evol. Syst., 38, 621-654. doi: 10.1146/annurev.ecolsys.36.102403.114735
[10] Buss, L. W. (1987). The Evolution of Individuality. Princeton, NJ: Princeton Univ. Press.
[11] Godfrey-Smith, P. (2009). Darwinian Populations and Natural Selection. Oxford University Press, USA.
[12] Van Gestel, J., and Tarnita, C. E. (2017). On the origin of biological construction, with a focus on multicellularity. Proceedings of the National Academy of Sciences, 114(42), 11018-11026. doi: 10.1073/pnas.1704631114
[13] Black, A. J., Bourrat, P., and Rainey, P. B. (2020). Ecological scaffolding and the evolution of individuality. Nature Ecology & Evolution, 4(3), 426-436. doi: 10.1038/s41559-019-1086-9
[14] Rose, C. J., Hammerschmidt, K., Pichugin, Y. and Rainey, P. B. (2020). Meta-population structure and the evolutionary transition to multicellularity. bioRxiv, 407163, ver. 5 peer-reviewed and recommended by PCI Evolutionary Biology. doi: 10.1101/407163

Meta-population structure and the evolutionary transition to multicellularityCaroline J Rose, Katrin Hammerschmidt, Yuriy Pichugin and Paul B Rainey<p>The evolutionary transition to multicellularity has occurred on numerous occasions, but transitions to complex life forms are rare. While the reasons are unclear, relevant factors include the intensity of within- versus between-group selection ...Adaptation, Evolutionary Dynamics, Experimental EvolutionDustin Brisson2019-04-04 12:26:36 View