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14 Dec 2016
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The Red Queen lives: epistasis between linked resistance loci

Evidence of epistasis provides further support to the Red Queen theory of host-parasite coevolution

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According to the Red Queen theory of antagonistic host-parasite coevolution, adaptation of parasites to the most common host genotype results in negative frequency-dependent selection whereby rare host genotypes are favoured. Assuming that host resistance relies on a genetic host-parasite (mis)match involving several linked loci, then recombination appears as much more efficient than parthenogenesis in generating new resistant host genotypes. This has long been proposed to explain one of the biggest so-called paradoxes in evolutionary biology, i.e. the maintenance of recombination despite its twofold cost.

Evidence from various study systems indicates that successful infection (and hence host resistance) depends on a genetic match between the parasite’s and the host’s genotype via molecular interactions involving elicitor/receptor mechanisms. However the key assumption of epistasis, i.e. that this genetic host-parasite match involves several linked resistance loci, remained unsupported so far. Metzger and coauthors [1] now provide empirical support for it.

Daphnia magna can reproduce both sexually and clonally and their well-studied interaction with Pasteuria ramosa makes them an excellent model system to investigate the genetics of host resistance. D. magna hosts were found to be either resistant (complete lack of attachment of parasite spores to the host’s foregut) or susceptible (full attachment). In this study the authors carried out an elegant Mendelian genetic investigation by performing multiple crosses between four host genotypes differing in their resistance to two different parasite isolates [1].

Their results show that resistance of D. magna to each of the two P. ramosa isolates relies on Mendelian inheritance at two loci that are linked (A and B), each of them having two alleles with dominant resistance; furthermore resistance to one parasite isolate confers susceptibility to the other. They also show that a third locus appears to confer double resistance (C), but that even double resistant hosts remain susceptible to other parasite isolates, and hence that universal host resistance is lacking – all of this supporting the Red Queen theory.

This paper demonstrates with a high level of clarity that host resistance is governed by multiple linked loci. The assumption of epistasis between resistance loci is supported, which makes it possible for sexual recombination to be maintained by antagonistic host-parasite coevolution.

Reference

[1] Metzger CMJA, Luijckx P, Bento G, Mariadassou M, Ebert D. 2016. The Red Queen lives: epistasis between linked resistance loci. Evolution 70:480-487. doi: 10.1111/evo.12854

The Red Queen lives: epistasis between linked resistance lociMetzger CMJA, Luijckx P, Bento G, Mariadassou M, Ebert D.A popular theory explaining the maintenance of genetic recombination (sex) is the Red Queen Theory. This theory revolves around the idea that time-lagged negative frequency-dependent selection by parasites favors rare host genotypes generated thro...Evolutionary Dynamics, Evolutionary Theory, Reproduction and Sex, Species interactionsAdele Mennerat2016-12-14 13:58:53 View
07 Aug 2023
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Pollen-feeding delays reproductive senescence and maintains toxicity of Heliconius erato

Impact of pollen-feeding on egg-laying and cyanogenic glucoside abundance in red postman butterflies

Recommended by based on reviews by Carol Boggs, Caroline Mueller and 1 anonymous reviewer

Growth, development and reproduction in animals are all limited by dietary nutrients. Expansion of an organism’s diet to sources not accessible to closely related species reduces food competition, and eases the constraints of nutrient-limited diets. Adult butterflies are herbivorous insects known to feed primarily on nectar from flowers, which is rich in sugars but poor in amino acids.  Only certain species in the genus Heliconius are known to also feed on pollen, which is especially rich in amino acids, and is known to prolong their lives by several months. The ability to digest pollen in Heliconius has been linked to specialized feeding behaviors (Krenn et al. 2009) and extra-oral digestion using enzymes, possibly including duplicated copies of cocoonase (Harpel et al. 2016; Smith et al. 2016 and 2018), a protease used by some moths to digest silk upon eclosion from their cocoons. In this reprint, Pinheiro de Castro and colleagues investigated the impact of artificial and natural diets on egg-laying ability, body weight, and cyanogenic glucoside abundance in adult Heliconius erato butterflies of both sexes. 

Previous studies (Dunlap-Pianka et al. 1981) in H. charithonia demonstrated that access to dietary pollen led to extended egg-laying ability among adult female butterflies compared to females deprived of pollen, and compared to Dryas iulia females which feed only on nectar. In the current study, Pinheiro de Castro et al. (2023) examine the impact of diet on both young and old H. erato, over a longer period of time than the earlier work, highlighting the importance of extending the time period over which effects are evaluated. In addition to extending egg-laying ability in older females, the authors found that pollen in the diet appeared to maintain older female body weight, presumably because the pollen contained nutrients depleted during egg-laying.

The authors then investigated the effects of nutrition on the production of cyanogenic glycoside defenses. Heliconius are aposematic butterflies that sequester cyanide-forming defense chemicals from food plants as larvae or synthesize these compounds de novo. The authors found the abundance of cyanogenic glycosides to be significantly greater in butterflies with access to pollen, but again only in older females.

Curiously, field studies of male and female H. charithonia butterflies found that females in the wild collected more pollen than males (Mendoza-Cuenca and Macías-Ordóñez 2005). Taken together, these new findings raise the intriguing possibility that females collect more pollen than males, in part, because pollen has a bigger impact on female survival and reproduction. A small limitation of the study is the use of wing length, rather than body weight, at the zero time point. But the trend is clear in both males and females, and it adds supporting detail to the efficacy of pollen feeding as an unusual strategy for increasing fertility and survival in Heliconius butterflies.

 

References
 
Dunlap-Pianka, Helen, Carol L. Boggs, Lawrence E. Gilbert. (1977) Ovarian dynamics in heliconiine butterflies: Programmed senescence versus eternal youth. Science, 197: 487-490, https://doi.org/10.1126/Science.197.4302.487
 
Pinheiro de Castro, Erika C., Josie McPherson, Glennis Julian, Anniina L. K. Mattila, Søren Bak, Stephen H. Montgomery, Chris Jiggins. (2023) Pollen-feeding delays reproductive senescence and maintains toxicity of Heliconius erato. bioRxiv, 2023.01.13.523799, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2023.01.13.523799
 
Krenn, Harald W., Monika J. B. Eberhard, Stefan H. Eberhard, Anna-Laetitia Hikl, Werner Huber, Lawrence E. Gilbert (2009). Mechanical damage to pollen aids nutrient acquisition in Heliconius butterflies (Nymphalidae).  Arthropod-Plant Interactions, 3: 203–208. https://doi.org/10.1007/s11829-009-9074-7
 
Harpel, Desiree, Darron A. Cullen, Swidbert R. Ott, Chris D. Jiggins, James R. Walters (2015) Pollen feeding proteomics: Salivary proteins of the passion flower butterfly, Heliconius melpomene. Insect Biochemistry and Molecular Biology, 63: 7-13, https://doi.org/10.1016/j.ibmb.2015.04.004
 
Mendoza-Cuenca, Luis, Rogelio Macías-Ordóñez (2005) Foraging polymorphism in Heliconius charitonia (Lepidoptera: Nymphalidae): morphological constraints and behavioral compensation. Journal of Tropical Ecology, 21: 407-415. https://doi.org/10.1017/S0266467405002385
 
Smith, Gilbert, Aide Macias-Muñoz, John Kelly, Carter Butts, Rachel Martin, Adriana D. Briscoe (2018) Evolutionary and structural analyses uncover a role for solvent interactions in the diversification of cocoonases in butterflies. Proceedings of the Royal Society B, 285: 20172037. https://doi.org/10.1098/rspb.2017.2037 
 
Smith, Gilbert, Aide Macias-Muñoz, Adriana D. Briscoe (2016) Gene duplication and gene expression changes play a role in the evolution of candidate pollen-feeding genes in Heliconius butterflies. Genome Biology and Evolution, 8: 2581-2596. https://doi.org/10.1093/gbe/evw180

Pollen-feeding delays reproductive senescence and maintains toxicity of Heliconius eratoErika C. Pinheiro de Castro, Josie McPherson, Glennis Jullian, Anniina L. K. Mattila, Søren Bak, Stephen Montgomery, Chris Jiggins<p>Dietary shifts may act to ease energetic constraints and allow organisms to optimise life-history traits. Heliconius butterflies differ from other nectar-feeders due to their unique ability to digest pollen, which provides a reliable source of ...Evolutionary Ecology, Life HistoryAdriana Briscoe2023-02-07 12:59:54 View
05 Oct 2022
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Do closely related species interact with similar partners? Testing for phylogenetic signal in bipartite interaction networks

Testing for phylogenetic signal in species interaction networks

Recommended by based on reviews by Joaquin Calatayud and Thomas Guillerme

Species are immersed within communities in which they interact mutualistically, as in pollination or seed dispersal, or nonreciprocally, such as in predation or parasitism, with other species and these interactions play a paramount role in shaping biodiversity (Bascompte and Jordano 2013). Researchers have become increasingly interested in the processes that shape these interactions and how these influence community structure and responses to disturbances. Species interactions are often described using bipartite interaction networks and one important question is how the evolutionary history of the species involved influences the network, including whether there is phylogenetic signal in interactions, in other words whether closely related species interact with other closely related species (Bascompte and Jordano 2013, Perez-Lamarque et al. 2022). To address this question different approaches, correlative and model-based, have been developed to test for phylogenetic signal in interactions, although comparative analyses of the performance of these different metrics are lacking. In their article Perez-Lamarque et al. (2022) set out to test the statistical performance of two widely-used methods, Mantel tests and Phylogenetic Bipartite Linear Models (PBLM; Ives and Godfray 2006) using simulations. Phylogenetic signal is measured as the degree to which distance to the nearest common ancestor predicts the observed similarity in trait values among species. In species interaction networks, the data are actually the between-species dissimilarity among interacting species (Perez-Lamarque et al. 2022), and typical approaches to test for phylogenetic signal cannot be used. However, the Mantel test provides a useful means of analyzing the correlation between two distance matrices, the between-species phylogenetic distance and the between-species dissimilarity in interactions. The PBLM approach, on the other hand, assumes that interactions between species are influenced by unobserved traits that evolve along the phylogenies following a given phenotypic evolution model and the parameters of this model are interpreted in terms of phylogenetic signal (Ives and Godfray 2006). Perez-Lamarque et al (2022) found that the model-based PBLM approach has a high type-I error rate, in other words it often detected phylogenetic signal when there was none. The simple Mantel test was found to present a low type-I error rate and moderate statistical power. However, it tended to overestimate the degree to which species interact with dissimilar partners. In addition to the aforementioned analyses, the authors also tested whether the simple Mantel test was able to detect phylogenetic signal in interactions among species within a given clade in the phylogeny, as phylogenetic signal in species interactions may be localized within specific clades. The article concludes with general guidelines for users wishing to test phylogenetic signal in their interaction networks and illustrates them with an example of an orchid-mycorrhizal fungus network from the oceanic island of La Réunion (Martos et al 2012). This broadly accessible article provides a valuable analysis of the performance of tests of phylogenetic signal in interaction networks enabling users to make informed choices of the analytical methods they wish to employ, and provide useful and detailed guidelines. Therefore, the work should be of broad interest to researchers studying species interactions.  

References

Bascompte J, Jordano P (2013) Mutualistic Networks. Princeton University Press. https://doi.org/10.1515/9781400848720

Ives AR, Godfray HCJ (2006) Phylogenetic Analysis of Trophic Associations. The American Naturalist, 168, E1–E14. https://doi.org/10.1086/505157

Martos F, Munoz F, Pailler T, Kottke I, Gonneau C, Selosse M-A (2012) The role of epiphytism in architecture and evolutionary constraint within mycorrhizal networks of tropical orchids. Molecular Ecology, 21, 5098–5109. https://doi.org/10.1111/j.1365-294X.2012.05692.x

Perez-Lamarque B, Maliet O, Pichon B, Selosse M-A, Martos F, Morlon H (2022) Do closely related species interact with similar partners? Testing for phylogenetic signal in bipartite interaction networks. bioRxiv, 2021.08.30.458192, ver. 6 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2021.08.30.458192

Do closely related species interact with similar partners? Testing for phylogenetic signal in bipartite interaction networks Benoît Perez-Lamarque, Odile Maliet, Benoît Pichon, Marc-André Selosse, Florent Martos, Hélène Morlon<p style="text-align: justify;">Whether interactions between species are conserved on evolutionary time-scales has spurred the development of both correlative and process-based approaches for testing phylogenetic signal in interspecific interactio...Evolutionary Ecology, Species interactionsAlejandro Gonzalez Voyer2022-03-10 13:48:15 View
13 Nov 2023
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Color polymorphism and conspicuousness do not increase speciation rates in Lacertids

Colour polymorphism does not increase diversification rates in lizards

Recommended by based on reviews by 2 anonymous reviewers

The striking differences in species richness among lineages in the Tree of Life have long attracted much research interest. In particular, researchers have asked whether certain traits are associated with greater diversification, with a particular focus on traits under sexual selection given their direct link to mating isolation.

Polymorphism, defined as the presence of co-occurring, heritable morphs within a population, has been proposed to influence diversification rates although the effect has been proposed as both promoting or alternatively impeding speciation. The effect of polymorphism may be positive, that is facilitating speciation if polymorphism allows to broaden the ecological niche, thus enabling range expansion, or enabling maintenance of populations in variable environments. Specialized ectomorphs have been observed in several species (e.g. Kusche et al. 2015, Lattanzio and Miles 2016, Whitney et al. 2018, Scali et al. 2016). Polymorphism may also facilitate speciation if a morph is lost during the colonization of a novel area or niche, resulting in rapid divergence of the remaining morphs and reproductive isolation from the ancestral population, known as the morph speciation hypothesis (West-Eberhard 1986, Corl et al. 2010). On the other hand, polymorphism may hamper speciation through disassortative maintaining by morph, which may maintain the polymorphism through the speciation process (Jamie and Meier 2020). An example of such a process is Heliconius numata where disassortative mate preferences based on color hampers ecological speciation (Chouteau et al. 2017). Previous evidence in birds and lizards suggests polymorphism favors diversification (Corl et al. 2010b, 2012, Hugall and Stuart-Fox 2012, Brock et al. 2021).

Here, de Solan et al. (2023) test the effect of polymorphism on diversification in Lacertidae, a family of lizards containing more than 300 species distributed across Europe, Africa and Asia. The group offers a good model system to test the effect of polymorphism on speciation as it contains several species with colour polymorphism, sometimes present in both sexes but restricted to males when present in the flank. Using coloration data from the literature as well as photographs of live specimens for 295 species the authors tested whether the presence of polymorphism is associated with higher diversification rates.

While undertaking their project, another group independently tackled the same question (Brock et al. 2021), using the same model system but coming to very different conclusions. Therefore, de Solan et al. (2023) decided to also contrast their results with those of Brock et al. (2021) to determine the factors responsible for the contrasting results of both studies. The latter I consider one of the strengths of the work, given the careful re-analyses to determine the causes of the discrepancies between both studies. De Solan et al. (2023) found no association between the presence of polymorphism and diversification rates, even though they used different analytical approaches. Thus, this study is interesting as it provides results that do not support a positive effect of polymorphism on species richness. The use of a phylogeny with more limited species sampling (García-Porta et al. 2019) implied that the authors had to manually add 75 species, of which 17 were added to the tree based on information from previously published trees and 68 were added at random locations within the genus. To control for potential biases the authors repeated the analyses using a sample of trees with the imputed taxa, results were broadly concordant across the set of trees. The careful re-analysis contrasting Brock et al. (2021) and de Solan et al. (2023) results suggests the difference is mainly due to a difference in how species were coded as presenting polymorphism, which differed between the two studies, as well as a difference in the package version used to run the state-dependent diversification models. Interestingly non-parametric analyses yielded similar results across both datasets. 
 
References
 
Brock, K.M., McTavish, E.J., Edwards, D.L. 2021. Colour polymorphism is a driver of diversification in the lizard family Lacertidae. Systematic Biology. 71: 24-39. https://doi.org/10.1093/sysbio/syab046
 
Chouteau, M., Llaurens, V., Piron-Prunier, F., Joron, M. 2017. Polymorphism at a mimicry supergene maintained by opposing frequency-dependent selection pressures. Proceedings of the National Academy of Sciences. 114: 8325-8329. https://doi.org/10.1073/pnas.1702482114
 
Corl, A., Davis, A.R., Kuchta, S.R., Comendant, T., Sinervo, B. 2010a. Alternative mating strategies and the evolution of sexual dimorphism in the side-blotched lizard, Uta stansburiana: a population-level comparative analysis. Evolution. 64: 79-96. https://doi.org/10.1111/j.1558-5646.2009.00791.x 
 
Corl, A., Davis, A.R., Kuchta, S.R., Sinervo, B. 2010b. Selective loss of polymorphic mating types is associated with rapid phenotypic evolution during morphic speciation. Proceedings of the National Academy of Sciences. 107: 4254-4259. https://doi.org/10.1073/pnas.0909480107
 
Corl, A., Lancaster, L.T., Sinervo, B. 2012. Rapid formation of reproductive isolation between two populations of side-blotched lizards, Uta stansburiana. Copeia. 2012: 593-602. https://doi.org/10.1643/CH-11-166

Garcia-Porta, J., Irisarri, I., Kirchner, M. et al. 2019. Environmental temperatures shape thermal physiology as well as diversification and genome-wide substitution rates in lizards. Nature Communications. 10: 4077. https://doi.org/10.1038/s41467-019-11943-x
 
Hugall, A.F., Stuart-Fox, D. 2012. Accelerated speciation in colour-polymorphic birds. Nature. 485: 631-634. https://doi.org/10.1038/nature11050
 
Jamie, G.A. and Meier, J.I. 2020. The persistence of polymorphisms across species radiations. Trends in Ecology and Evolution. 35: 795-808. https://doi.org/10.1016/j.tree.2020.04.007
 
Kusche, H., Elmer, K.R., Meyer, A. 2015. Sympatric ecological divergence associated with a colour polymorphism. BMC Biology, 13: 82. https://doi.org/10.1186/s12915-015-0192-7
 
Lattanzio, M.S. and Miles, D.B. 2016. Trophic niche divergence among colour morphs that exhibit alternative mating tactics. Royal Society Open Science. 3: 150531. https://doi.org/10.1098/rsos.150531
 
Scali, S., Sacchi, R., Mangiacotti, M., Pupin, F., Gentilli, A., Zucchi, C. Scannolo, M., Pavesi, M., Zuffi, M.A.L. 2016. Does a polymorphic species have a ‘polymorphic’ diet? A case study from a lacertid lizard. Biologcial Journal of the Linnean Society. 117: 492-502. https://doi.org/10.1111/bij.12652

de Solan T, Sinervo B, Geniez P, David P, Crochet P-A (2023) Colour polymorphism and conspicuousness do not increase speciation rates in Lacertids. bioRxiv, 2023.02.15.528678, ver. 2 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2023.02.15.528678

West-Eberhard, M.J. 1986. Alternative adaptations, speciation, and phylogeny (A review). Proceedings of the National Academy of Sciences. 83: 1388-1392. https://doi.org/10.1073/pnas.83.5.1388
 
Whitney, J.L., Donahue, M.J., Karl, S.A. 2018. Niche divergence along a fine-scale ecological gradient in sympatric colour morphs of a coral reef fish. Ecosphere. 9: e02015. https://doi.org/10.1002/ecs2.2015

Color polymorphism and conspicuousness do not increase speciation rates in LacertidsThomas de Solan, Barry Sinervo, Philippe Geniez, Patrice David, Pierre-André Crochet<p style="text-align: justify;">Conspicuous body colors and color polymorphism have been hypothesized to increase rates of speciation. Conspicuous colors are evolutionary labile, and often involved in intraspecific sexual signaling and thus may pr...Evolutionary Ecology, Macroevolution, SpeciationAlejandro Gonzalez Voyer2023-02-22 10:05:03 View
14 Dec 2016
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Evolution of resistance to single and combined floral phytochemicals by a bumble bee parasite

The medicinal value of phytochemicals is hindered by pathogen evolution of resistance

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As plants cannot run from their enemies, natural selection has favoured the evolution of diverse chemical compounds (phytochemicals) to protect them against herbivores and pathogens. This provides an opportunity for plant feeders to exploit these compounds to combat their own enemies. Indeed, it is widely known that herbivores use such compounds as protection against predators [1]. Recently, this reasoning has been extended to pathogens, and elegant studies have shown that some herbivores feed on phytochemical-containing plants reducing both parasite abundance within hosts [2] and their virulence [3].
Suffering less from parasites is clearly beneficial for infected herbivores. Why then, is this behaviour not fixed in nature? There are, at least, two possible explanations. First, feeding on ‘medicinal’, often toxic, plants may impose costs upon uninfected individuals. Second, parasites may evolve resistance to such chemicals. Whereas the first possibility has been explored, and is taken as evidence for ‘self-medication’ [3], the second hypothesis requires investigation. A recent study by Palmer-Young et al. [4] fills this gap. This article reports evolution of resistance to two different phytochemicals, alone and in combination, in the trypanosome Crithidia bombi, a bumble bee (Bombus impatiens) parasite. To show this, the authors experimentally evolved a strain of C. bombi in the presence of thymol, eugenol or both simultaneously. These phytochemicals are commonly found in the nectar of several plant species, in particular those of the Lamiaceae, a family containing several aromatic herbs. Prior to selection both phytochemicals reduced C. bombi growth by about 50%. However, C. bombi rapidly evolved resistance in both single and the double phytochemical treatments. Moreover, no cost of resistance was detected when evolved parasites were placed in the ancestral, phytochemical-free environment. Therefore, resistance to phytochemicals would be expected to spread rapidly in natural populations of C. bombi. Clearly, thus, the herbivore strategy of sequestering plant secondary chemical compounds as a defence against their pathogens should fail. The question then is ‘why do they still do it’? Can self-medication work in the longer-term for bumblebees?
Well, yes. The very fact that resistance evolved shows that resistance is not fixed in natural C. bombi populations. This is surprising considering that resistance is not costly. This might be due to a number of reasons. Firstly, there may be costs of resistance that were not detected in this experiment. Second, it may not be possible to evolve universal resistance to the heterogeneity present in the phytochemical environment. Indeed, phytochemical environments are highly varied in time and space and bumblebees will visit different plants presenting different phytochemical cocktails throughout the season. Furthermore, migration of bees from populations exposed to different phytochemicals may prevent the fixation of one resistance type.
Or, it may be self-medication behaviour itself that prevents the evolution of resistance? Indeed, in the same way that infected bees seek cooler temperatures to slow growth of a parasitoid fly [5], they may also seek a more varied diet with diverse phytochemicals to which the parasite cannot evolve, but which reduces parasite growth. Further understanding of arthropod self-medication may thus be instrumental to prevent the observed worldwide decline of pollinators [6]. Furthermore, it may inform on mechanisms that prevent rapid evolution of drug resistance in other systems.

References

[1] Duffey SS. 1980. Sequestration of plant natural products by insects. Annual Review of Entomology 25: 447-477. doi: 10.1146/annurev.en.25.010180.002311

[2] Richardson LL et al. 2015. Secondary metabolites in floral nectar reduce parasite infections in bumblebees. Proceedings of the Royal Society of London B 282: 20142471. doi: 10.1098/rspb.2014.2471

[3] Lefèvre T et al. 2010. Evidence for trans-generational medication in nature. Ecology Letters 13: 1485-93. doi: 10.1111/j.1461-0248.2010.01537.x

[4] Palmer-Young EC, Sadd BM, Adler LS. 2017. Evolution of resistance to single and combined floral phytochemicals by a bumble bee parasite. Journal of Evolutionary Biology 30: 300-312. doi: 10.1111/jeb.13002

[5] Müller CB, Schmid-Hempel P. 1993. Exploitation of cold temperature as defence against parasitoids in bumblebees. Nature 363: 65-67. doi: 10.1038/363065a0

[6] Potts SG et al. 2010. Global pollinator declines: trends, impacts and drivers. Trends in Ecology and Evolution 25: 345-353. doi: 10.1016/j.tree.2010.01.007

Evolution of resistance to single and combined floral phytochemicals by a bumble bee parasitePalmer-Young EC, Sadd BM, Adler LSRepeated exposure to inhibitory compounds can drive the evolution of resistance, which weakens chemical defence against antagonists. Floral phytochemicals in nectar and pollen have antimicrobial properties that can ameliorate infection in pollinat...Evolutionary EcologyAlison Duncan2016-12-14 16:47:14 View
09 Nov 2018
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Field evidence for manipulation of mosquito host selection by the human malaria parasite, Plasmodium falciparum

Malaria host manipulation increases probability of mosquitoes feeding on humans

Recommended by based on reviews by Olivier Restif, Ricardo S. Ramiro and 1 anonymous reviewer

Parasites can manipulate their host’s behaviour to ensure their own transmission. These manipulated behaviours may be outside the range of ordinary host activities [1], or alter the crucial timing and/or location of a host’s regular activity. Vantaux et al show that the latter is true for the human malaria parasite, Plasmodium falciparum [2]. They demonstrate that three species of Anopheles mosquito were 24% more likely to choose human hosts, rather than other vertebrates, for their blood feed when they harboured transmissible stages (sporozoites) compared to when they were uninfected, or infected with non-transmissible malaria parasites [2]. Host choice is crucial for the malaria parasite Plasmodium falciparum to complete its life-cycle, as their host range is much narrower than the mosquito’s for feeding; P. falciparum can only develop in hominids, or closely related apes [3].
The study only shows this stage-dependent parasite manipulation retrospectively (by identifying host type and parasite stage in mosquitoes after their blood feed [2]). There was no difference in the preferences of infectious (with sporozoites) or un-infectious (infected without sporozoites, or uninfected) mosquitoes between human versus cow hosts in a choice test [2]. This suggests that the final decision about whether to feed occurs when the mosquito is in close range of the host.
This, coupled with previous findings, shows that vector manipulation is a fine-tuned business, that can act at multiple stages of the parasite life-cycle and on many behaviours [4]. Indeed, mosquitoes with non-transmissible Plasmodium stages (oocysts) are more reluctant to feed than sporozoite-infected mosquitoes [5] as vectors can be killed by their host whilst feeding, doing so before they are ready to transmit is risky for the malaria parasite. Thus, it seems that Plasmodium is, to some extent, master of its vector; commanding it not to feed when it cannot be transmitted, to feed when it is ready to be transmitted and to feed on the right type of host. What does this mean for our understanding of malaria transmission and epidemics?
Vantaux et al use a mathematical model, parameterised using data from this experiment, to highlight the consequences of this 24% increase in feeding on humans for P. falciparum transmission. They show that this increase raises the number of infectious bites humans receive from 4 (if sporozoite-infected mosquitoes had the same probability as uninfected mosquitoes) to 14 (an increase in 250%), for mosquitoes with a 15-day life-span, at ratios of 1:1 mosquitoes to humans. Longer mosquito life-spans and higher ratios of mosquitoes to humans further increases the number of infectious bites.
These results [2] have important implications for epidemiological forecasting and disease management. Public health strategies could focus on possible ways to trap sporozoite-infected mosquitoes, mimicking cues they use to locate their human hosts, or identify the behaviour of mosquitoes harbouring non-yet infectious Plasmodium, and trap them before they bite. Moreover, the results of the model show that failing to take into account the preference for humans of sporozoite-infected mosquitoes could underestimate the size of pending epidemics.
An important question previously raised is whether Plasmodium-induced alteration in host behaviour really is manipulation, or just a side-effect of being infected [4,5]. The fact that Vantaux et al show that these altered feeding behaviours increases the likelihood of transmission, in that a sporozoite-infected mosquito is more likely to feed on a human, strongly suggests that it is adaptive for the parasite [2]. Ultimately, to show that it is manipulation would require the identification of molecular factors released by Plasmodium that are responsible for physiological changes in the mosquito [6].

References

[1] Thomas, F., Schmidt-Rhaesa, A., Martin, G., Manu, C., Durand, P., & Renaud, F. (2002). Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts? Journal of Evolutionary Biology, 15(3), 356–361. doi: 10.1046/j.1420-9101.2002.00410.x
[2] Vantaux, A., Yao, F., Hien, D. F., Guissou, E., Yameogo, B. K., Gouagna, L.-C., … Lefevre, T. (2018). Field evidence for manipulation of mosquito host selection by the human malaria parasite, Plasmodium falciparum. BioRxiv, 207183 ver 6. doi: 10.1101/207183
[3] Prugnolle, F., Durand, P., Ollomo, B., Duval, L., Ariey, F., Arnathau, C., … Renaud, F. (2011). A Fresh Look at the Origin of Plasmodium falciparum, the Most Malignant Malaria Agent. PLOS Pathogens, 7(2), e1001283. doi: 10.1371/journal.ppat.1001283
[4] Cator, L. J., Lynch, P. A., Read, A. F., & Thomas, M. B. (2012). Do malaria parasites manipulate mosquitoes? Trends in Parasitology, 28(11), 466–470. doi: 10.1016/j.pt.2012.08.004
[5] Cator, L. J., George, J., Blanford, S., Murdock, C. C., Baker, T. C., Read, A. F., & Thomas, M. B. (2013). “Manipulation” without the parasite: altered feeding behaviour of mosquitoes is not dependent on infection with malaria parasites. Proceedings. Biological Sciences, 280(1763), 20130711. doi: 10.1098/rspb.2013.0711
[6] Herbison, R., Lagrue, C., & Poulin, R. (2018). The missing link in parasite manipulation of host behaviour. Parasites & Vectors, 11. doi: 10.1186/s13071-018-2805-9

Field evidence for manipulation of mosquito host selection by the human malaria parasite, Plasmodium falciparumAmelie Vantaux, Franck Yao, Domonbabele FdS Hien, Edwige Guissou, Bienvenue K Yameogo, Louis-Clement Gouagna, Didier Fontenille, Francois Renaud, Frederic Simard, Carlo Constantini, Frederic Thomas, Karine Mouline, Benjamin Roche, Anna Cohuet, Kou...<p>Whether the malaria parasite *Plasmodium falciparum* can manipulate mosquito host choice in ways that enhance parasite transmission toward human is unknown. We assessed the influence of *P. falciparum* on the blood-feeding behaviour of three of...Evolutionary EcologyAlison Duncan2018-02-28 09:12:14 View
11 May 2021
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Wolbachia load variation in Drosophila is more likely caused by drift than by host genetic factors

Drift rather than host or parasite control can explain within-host Wolbachia growth

Recommended by and based on reviews by Simon Fellous and 1 anonymous reviewer

Within-host parasite density is tightly linked to parasite fitness often determining both transmission success and virulence (parasite-induced harm to the host) (Alizon et al., 2009, Anderson & May, 1982). Parasite density may thus be controlled by selection balancing these conflicting pressures. Actual within-host density regulation may be under host or parasite control, or due to other environmental factors (Wale et al., 2019, Vale et al., 2011, Chrostek et al., 2013). Vertically transmitted parasites may also be more vulnerable to drift associated with bottlenecks between generations, which may also determine within-host population size (Mathe-Hubert et al., 2019, Mira & Moran, 2002).

Bénard et al. (2021) use 3 experiments to disentangle the role of drift versus host factors in the control of within-host Wolbachia growth in Drosophila melanogaster. They use the wMelPop Wolbachia strain in which virulence (fly longevity) and within-host growth correlate positively with copy number in the genomic region Octomom (Chrostek et al., 2013, Chrostek & Teixeira, 2015). Octomom copy number can be used as a marker for different genetic lineages within the wMelPop strain.

In a first experiment, they introgressed and backcrossed this Wolbachia strain into 6 different host genetic backgrounds and show striking differences in within-host symbiont densities which correlate positively with Octomom copy number. This is consistent with host genotype selecting different Wolbachia strains, but also with bottlenecks and drift between generations. To distinguish between these possibilities, they perform 2 further experiments. 

A second experiment repeated experiment 1, but this time introgression was into 3 independent lines of the Bolivia and USA Drosophila populations; those that, respectively, exhibited the lowest and highest Wolbachia density and Octomom copy number. In this experiment, growth and Octomom copy number were measured across the 3 lines, for each population, after 1, 13 and 25 generations. Although there were little differences between replicates at generation 1, there were differences at generations 13 and 25 among the replicates of both the Bolivia and USA lines. These results are indicative of parasite control, or drift being responsible for within-host growth rather than host factors. 

A third experiment tested whether Wolbachia density and copy number were under host or parasite control. This was done, again using the USA and Bolivia lines, but this time those from the first experiment, several generations following the initial introgression and backcrossing. The newly introgressed lines were again followed for 25 generations. At generation 1, Wolbachia phenotypes resembled those of the donor parasite population and not the recipient host population indicating a possible maternal effect, but a lack of host control over the parasite. Furthermore, Wolbachia densities and Octomom number differed among replicate lines through time for Bolivia populations and from the donor parasite lines for both populations. These differences among replicate lines that share both host and parasite origins suggest that drift and/or maternal effects are responsible for within-host Wolbachia density and Octomom number. 

These findings indicate that drift appears to play a role in shaping Wolbachia evolution in this system. Nevertheless, completely ruling out the role of the host or parasite in controlling densities will require further study. The findings of Bénard and coworkers (2021) should stimulate future work on the contribution of drift to the evolution of vertically transmitted parasites.

References

Alizon S, Hurford A, Mideo N, Baalen MV (2009) Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. Journal of Evolutionary Biology, 22, 245–259. https://doi.org/10.1111/j.1420-9101.2008.01658.x

Anderson RM, May RM (1982) Coevolution of hosts and parasites. Parasitology, 85, 411–426. https://doi.org/10.1017/S0031182000055360

Bénard A, Henri H, Noûs C, Vavre F, Kremer N (2021) Wolbachia load variation in Drosophila is more likely caused by drift than by host genetic factors. bioRxiv, 2020.11.29.402545, ver. 4  recommended and peer-reviewed by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2020.11.29.402545

Chrostek E, Marialva MSP, Esteves SS, Weinert LA, Martinez J, Jiggins FM, Teixeira L (2013) Wolbachia Variants Induce Differential Protection to Viruses in Drosophila melanogaster: A Phenotypic and Phylogenomic Analysis. PLOS Genetics, 9, e1003896. https://doi.org/10.1371/journal.pgen.1003896

Chrostek E, Teixeira L (2015) Mutualism Breakdown by Amplification of Wolbachia Genes. PLOS Biology, 13, e1002065. https://doi.org/10.1371/journal.pbio.1002065

Mathé‐Hubert H, Kaech H, Hertaeg C, Jaenike J, Vorburger C (2019) Nonrandom associations of maternally transmitted symbionts in insects: The roles of drift versus biased cotransmission and selection. Molecular Ecology, 28, 5330–5346. https://doi.org/10.1111/mec.15206

Mira A, Moran NA (2002) Estimating Population Size and Transmission Bottlenecks in Maternally Transmitted Endosymbiotic Bacteria. Microbial Ecology, 44, 137–143. https://doi.org/10.1007/s00248-002-0012-9

Vale PF, Wilson AJ, Best A, Boots M, Little TJ (2011) Epidemiological, Evolutionary, and Coevolutionary Implications of Context-Dependent Parasitism. The American Naturalist, 177, 510–521. https://doi.org/10.1086/659002

Wale N, Jones MJ, Sim DG, Read AF, King AA (2019) The contribution of host cell-directed vs. parasite-directed immunity to the disease and dynamics of malaria infections. Proceedings of the National Academy of Sciences, 116, 22386–22392. https://doi.org/10.1073/pnas.1908147116

 

Wolbachia load variation in Drosophila is more likely caused by drift than by host genetic factorsAlexis Bénard, Hélène Henri, Camille Noûs, Fabrice Vavre, Natacha Kremer <p style="text-align: justify;">Symbiosis is a continuum of long-term interactions ranging from mutualism to parasitism, according to the balance between costs and benefits for the protagonists. The density of endosymbionts is, in both cases, a ke...Evolutionary Dynamics, Genetic conflicts, Species interactionsAlison Duncan2020-12-01 16:28:14 View
02 Feb 2023
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Heterogeneities in infection outcomes across species: sex and tissue differences in virus susceptibility

Susceptibility to infection is not explained by sex or differences in tissue tropism across different species of Drosophila

Recommended by based on reviews by Greg Hurst and 1 anonymous reviewer

Understanding factors explaining both intra and interspecific variation in susceptibility to infection by parasites remains a key question in evolutionary biology. Within a species variation in susceptibility is often explained by differences in behaviour affecting exposure to infection and/or resistance affecting the degree by which parasite growth is controlled (Roy & Kirchner, 2000, Behringer et al., 2000). This can vary between the sexes (Kelly et al., 2018) and may be explained by the ability of a parasite to attack different organs or tissues (Brierley et al., 2019). However, what goes on within one species is not always relevant to another, making it unclear when patterns can be scaled up and generalised across species. This is also important to understand when parasites may jump hosts, or identify species that may be susceptible to a host jump (Longdon et al., 2015). Phylogenetic distance between hosts is often an important factor explaining susceptibility to a particular parasite in plant and animal hosts (Gilbert & Webb, 2007, Faria et al., 2013). 

In two separate experiments, Roberts and Longdon (Roberts & Longdon, 2022) investigated how sex and tissue tropism affected variation in the load of Drosophila C Virus (DCV) across multiple Drosophila species. DCV load has been shown to correlate positively with mortality (Longdon et al., 2015). Overall, they found that load did not vary between the sexes; within a species males and females had similar DCV loads for 31 different species. There was some variation in levels of DCV growth in different tissue types, but these too were consistent across males for 7 species of Drosophila. Instead, in both experiments, host phylogeny or interspecific variation, explained differences in DCV load with some species being more infected than others. 

This study is neat in that it incorporates and explores simultaneously both intra and interspecific variation in infection-related life-history traits which is not often done (but see (Longdon et al., 2015, Imrie et al., 2021, Longdon et al., 2011, Johnson et al., 2012). Indeed, most studies to date explore either inter-specific differences in susceptibility to a parasite (it can or can’t infect a given species) (Davies & Pedersen, 2008, Pfenning-Butterworth et al., 2021) or intra-specific variability in infection-related traits (infectivity, resistance etc.) due to factors such as sex, genotype and environment (Vale et al., 2008, Lambrechts et al., 2006). This work thus advances on previous studies, while at the same time showing that sex differences in parasite load are not necessarily pervasive. 

References

Behringer DC, Butler MJ, Shields JD (2006) Avoidance of disease by social lobsters. Nature, 441, 421–421. https://doi.org/10.1038/441421a

Brierley L, Pedersen AB, Woolhouse MEJ (2019) Tissue tropism and transmission ecology predict virulence of human RNA viruses. PLOS Biology, 17, e3000206. https://doi.org/10.1371/journal.pbio.3000206

Davies TJ, Pedersen AB (2008) Phylogeny and geography predict pathogen community similarity in wild primates and humans. Proceedings of the Royal Society B: Biological Sciences, 275, 1695–1701. https://doi.org/10.1098/rspb.2008.0284

Faria NR, Suchard MA, Rambaut A, Streicker DG, Lemey P (2013) Simultaneously reconstructing viral cross-species transmission history and identifying the underlying constraints. Philosophical Transactions of the Royal Society B: Biological Sciences, 368, 20120196. https://doi.org/10.1098/rstb.2012.0196

Gilbert GS, Webb CO (2007) Phylogenetic signal in plant pathogen–host range. Proceedings of the National Academy of Sciences, 104, 4979–4983. https://doi.org/10.1073/pnas.0607968104

Imrie RM, Roberts KE, Longdon B (2021) Between virus correlations in the outcome of infection across host species: Evidence of virus by host species interactions. Evolution Letters, 5, 472–483. https://doi.org/10.1002/evl3.247

Johnson PTJ, Rohr JR, Hoverman JT, Kellermanns E, Bowerman J, Lunde KB (2012) Living fast and dying of infection: host life history drives interspecific variation in infection and disease risk. Ecology Letters, 15, 235–242. https://doi.org/10.1111/j.1461-0248.2011.01730.x

Kelly CD, Stoehr AM, Nunn C, Smyth KN, Prokop ZM (2018) Sexual dimorphism in immunity across animals: a meta-analysis. Ecology Letters, 21, 1885–1894. https://doi.org/10.1111/ele.13164

Lambrechts L, Chavatte J-M, Snounou G, Koella JC (2006) Environmental influence on the genetic basis of mosquito resistance to malaria parasites. Proceedings of the Royal Society B: Biological Sciences, 273, 1501–1506. https://doi.org/10.1098/rspb.2006.3483

Longdon B, Hadfield JD, Day JP, Smith SCL, McGonigle JE, Cogni R, Cao C, Jiggins FM (2015) The Causes and Consequences of Changes in Virulence following Pathogen Host Shifts. PLOS Pathogens, 11, e1004728. https://doi.org/10.1371/journal.ppat.1004728

Longdon B, Hadfield JD, Webster CL, Obbard DJ, Jiggins FM (2011) Host Phylogeny Determines Viral Persistence and Replication in Novel Hosts. PLOS Pathogens, 7, e1002260. https://doi.org/10.1371/journal.ppat.1002260

Pfenning-Butterworth AC, Davies TJ, Cressler CE (2021) Identifying co-phylogenetic hotspots for zoonotic disease. Philosophical Transactions of the Royal Society B: Biological Sciences, 376, 20200363. https://doi.org/10.1098/rstb.2020.0363

Roberts KE, Longdon B (2023) Heterogeneities in infection outcomes across species: examining sex and tissue differences in virus susceptibility. bioRxiv 2022.11.01.514663, ver. 2 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.11.01.514663 

Roy BA, Kirchner JW (2000) Evolutionary Dynamics of Pathogen Resistance and Tolerance. Evolution, 54, 51–63. https://doi.org/10.1111/j.0014-3820.2000.tb00007.x

Vale PF, Stjernman M, Little TJ (2008) Temperature-dependent costs of parasitism and maintenance of polymorphism under genotype-by-environment interactions. Journal of Evolutionary Biology, 21, 1418–1427. https://doi.org/10.1111/j.1420-9101.2008.01555.x

Heterogeneities in infection outcomes across species: sex and tissue differences in virus susceptibilityKatherine E Roberts, Ben Longdon<p style="text-align: justify;">Species vary in their susceptibility to pathogens, and this can alter the ability of a pathogen to infect a novel host. However, many factors can generate heterogeneity in infection outcomes, obscuring our ability t...Evolutionary EcologyAlison DuncanAnonymous, Greg Hurst2022-11-03 11:17:42 View
13 Dec 2016
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Addicted? Reduced host resistance in populations with defensive symbionts

Hooked on Wolbachia

Recommended by and

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 FMHeritable 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 genes ...Adaptation, Evolutionary Applications, Evolutionary Ecology, Experimental Evolution, Life HistoryAna Rivero2016-12-13 20:08:37 View
20 Sep 2017
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An interaction between cancer progression and social environment in Drosophila

Cancer and loneliness in Drosophila

Recommended by based on reviews by Ana Rivero and Silvie Huijben

Drosophila flies may not be perceived as a quintessentially social animal, particularly when compared to their eusocial hymenopteran cousins. Although they have no parental care, division of labour or subfertile caste, fruit flies nevertheless exhibit an array of social phenotypes that are potentially comparable to those of their highly social relatives. In the wild, Drosophila adults cluster around food resources where courtship, mating activity and oviposition occur. Recent work has shown not only that social interactions in these clusters condition many aspects of the behaviour and physiology of the flies [1] but also, and perhaps more unexpectedly, that social isolation has a negative impact on their fitness [2].

Many studies in humans point to the role of social isolation as a source of stress that can induce and accelerate disease progression. The ultimate proof of the connection between social interaction and disease is however mired in confounding variables and alternative explanations so the subject, though crucial, remains controversial. With a series of elegant experiments using Drosophila flies that develop an inducible form of intestinal cancer, Dawson et al [3] show that cancer progresses more rapidly in flies maintained in isolation than in flies maintained with other cancerous flies. Further, cancerous flies kept with non-cancerous flies, fare just as badly as when kept alone. Their experiments suggest that this is due to the combined effect of healthy flies avoiding contact with cancerous flies (even though this is a non-contagious disease), and of cancerous flies having higher quality interactions with other cancerous flies than with healthy ones. Perceived isolation is therefore as pernicious as real isolation when it comes to cancer progression in these flies. Like all good research, this study opens up as many questions as it answers, in particular the why and wherefores of the flies’ extraordinary social behaviour in the face of disease.

References

[1] Camiletti AL and Thompson GJ. 2016. Drosophila as a genetically tractable model for social insect behavior. Frontiers in Ecology and Evolution, 4: 40. doi: 10.3389/fevo.2016.00040

[2] Ruan H and Wu C-F. 2008. Social interaction-mediated lifespan extension of Drosophila Cu/Zn superoxide dismutase mutants. Proceedings of the National Academy of Sciences, USA, 105: 7506-7510. doi: 10.1073/pnas.0711127105

[3] Dawson E, Bailly T, Dos Santos J, Moreno C, Devilliers M, Maroni B, Sueur C, Casali A, Ujvari B, Thomas F, Montagne J, Mery F. 2017. An interaction between cancer progression and social environment in Drosophila. BiorXiv, 143560, ver. 3 of 19th September 2017. doi: 10.1101/143560

An interaction between cancer progression and social environment in DrosophilaErika H. Dawson, Tiphaine P.M. Bailly, Julie Dos Santos , Céline Moreno, Maëlle Devilliers, Brigitte Maroni, Cédric Sueur, Andreu Casali, Beata Ujvari, Frederic Thomas, Jacques Montagne, Frederic MeryThe ecological benefits of sociality in gregarious species are widely acknowledged. However, only limited data is available on how the social environment influences non-communicable disease outcomes. For instance, despite extensive research over t...Behavior & Social Evolution, Evolutionary Ecology, Phenotypic PlasticityAna Rivero2017-05-30 08:55:16 View