In most animal species, males and females display distinct survival prospect, a phenomenon known as sex gap in longevity (SGL, Marais et al. 2018). The study of SGLs is crucial not only for having a full picture of the causes underlying organisms’ health, aging and death but also to initiate the development of sex-specific anti-aging interventions in humans (Austad and Bartke 2015). Three non-mutually evolutionary causes have been proposed to underlie SGLs (Marais et al. 2018). First, SGLs could be the consequences of sex-differences in life history strategies. For example, evolving dimorphic traits (e.g. body size, ornaments or armaments) may imply unequal physiological costs (e.g. developmental, maintenance) between the sexes and this may result in differences in longevity and aging. Second, mitochondria are usually transmitted by the mother and thus selection is blind to mitochondrial deleterious mutations affecting only males. Such mutations can freely accumulate in the mitochondrial genome and may reduce male longevity, a phenomenon called the mother’s curse (Frank and Hurst 1996). Third, in species with sex chromosomes, all recessive deleterious mutations will be expressed on the single X chromosome in XY males and may reduce their longevity (the unguarded X effect). In addition, the numerous transposable elements (TEs) on the Y chromosome may affect aging. TE activity is normally repressed by epigenetic regulation (DNA methylation, histone modifications and small RNAs). However, it is known that this regulation is disrupted with increasing age. Because of the TE-rich Y chromosome, more TEs may become active in old males than in old females, generating more somatic mutations, accelerating aging and reducing longevity in males (the toxic Y effect, Marais et al. 2018).
The relative contributions of these different effects to SGLs remain unknown. Sex-differences in life history strategies have been considered as the most important cause of SGLs for long (Tidière et al. 2015) but this effect remain equivocal (Lemaître et al. 2020) and cannot explain alone the diversity of patterns observed across species (Marais et al. 2018). Similarly, while studies in Drosophila and humans have shown that the mother’s curse contributes to SGLs in those organisms (e.g. Milot et al. 2007), its contribution may not be strong. Recently, two large-scale comparative analyses have shown that in species with XY chromosomes males show a shorter lifespan compared to females, while in species with ZW chromosomes (a system in which the female are the heterogametic sex and are ZW, and the males ZZ) the opposite pattern is observed (Pipoly et al. 2015; Xirocostas et al. 2020). Apart from these correlational studies, very little experimental tests of the effect of sex chromosomes on longevity have been conducted. In Drosophila, the evidence suggests that the unguarded X effect does not contribute to SGLs (Brengdahl et al. 2018). Whether a toxic Y effect exists in this species was unknown.
In a very elegant study, Brown et al. (2020) provided strong evidence for such a toxic Y effect in Drosophila melanogaster. First, they checked that in the D. melanogaster strain that they were studying (Canton-S), males were indeed dying younger than females. They also confirmed that in this strain, as in others, the male genomes include more repeats and heterochromatin than the female ones using cytometry. A careful analysis of the heterochromatin (using H3K9me2, a repressive histone modification typical of heterochromatin, as a proxy) in old flies revealed that heterochromatin loss was much more important in males than in females, in particular on the Y chromosome (but also to a lesser extent at the pericentromric regions of the autosomes). This change in heterochromatin had two outputs, they found. First, the expression of the genes in those regions was affected. They highlighted that many of such genes are involved in immunity and regulation with a potential impact on longevity. Second, they found a striking TE reactivation. These two effects were stronger in males. While females showed clear reactivation of 6 TEs, with the total fraction of repeats in the transcriptome going from 2% (young females) to 4.6% (old females), males experienced the reactivation of 32 TEs, with the total fraction of repeats in the transcriptome going from 1.6% (young males) to 5.8% (old males). It appeared that most of these TEs are Y-linked. And when focusing on Y-linked repeats, they found that 32 Y-linked TEs became upregulated during male aging and the fraction of Y-linked TEs in the transcriptome increased ninefold.
All these observations clearly suggested that male longevity was decreased because of a toxic Y effect. To really uncover a causal relationship between having a Y chromosome and shorter longevity, Brown et al. (2020) artificially produced flies with atypical karyotypes: X0 males, XXY females and XYY males. This is very interesting as they could uncouple the effect of the phenotypical sex (being male or female) and having a Y chromosome or not, as in fruit flies sex is determined not by the Y chromosome but by the X/autosome ratio. Their results are striking. They found that longevity of the X0 males was the highest (higher than XX females in fact), and that of the XYY males the lowest. Females XXY had intermediate longevities. Importantly, this was found to be robust to genomic background as results were the same using crosses from different strains. When analysing TEs of these flies, they found a particularly strong expression of the Y-linked TEs in old XXY and XYY flies. Interestingly, in young XXY and XYY flies Y-linked TEs expression was also strong, suggesting the chromatin regulation of the Y chromosome is disrupted in these flies.
This work points to the idea that SGLs in D. melanogaster are mainly explained by the toxic Y effect. The molecular details however remain to be elucidated. The effect of the Y chromosome on aging might be more complex than envisioned in the toxic Y model presented above. Brown et al. (2020) indeed found that heterochromatin loss was globally faster in males, both at the Y chromosome and the autosomes. The organisation of the nucleus, in particular of the nucleolus, which is involved in heterochromatin maintenance, involves the sex chromosomes in D. melanogaster as discussed in the paper, and may explain this observation. The epigenetic status of the Y chromosome is known to affect that of all the autosomes in Drosophila (Lemos et al. 2008). Also, in Brown et al. (2020) most of the work (in particular the genomic part) has been done on Canton-S. Only D. melanogaster was studied but limited data suggest different Drosophila species may have different SGLs. The TE analysis is known to be tricky, different tools to analyse TE expression exist (e.g. Lerat et al. 2017; Lanciano and Cristofari 2020). Future work should focus on testing the toxic Y effect on other D. melanogaster strains and other Drosophila species, using different tools to study TE expression, and on dissecting the molecular details of the toxic Y effect.

References

Austad, S. N., and Bartke, A. (2015). Sex differences in longevity and in responses to anti-aging interventions: A Mini-Review. Gerontology, 62(1), 40–46. 10.1159/000381472
Brengdahl, M., Kimber, C. M., Maguire-Baxter, J., and Friberg, U. (2018). Sex differences in life span: Females homozygous for the X chromosome do not suffer the shorter life span predicted by the unguarded X hypothesis. Evolution; international journal of organic evolution, 72(3), 568–577. 10.1111/evo.13434
Brown, E. J., Nguyen, A. H., and Bachtrog, D. (2020). The Y chromosome may contribute to sex-specific ageing in Drosophila. Nature ecology and evolution, 4(6), 853–862. 10.1038/s41559-020-1179-5 or preprint link on bioRxiv
Frank, S. A., and Hurst, L. D. (1996). Mitochondria and male disease. Nature, 383(6597), 224. 10.1038/383224a0
Lanciano, S., and Cristofari, G. (2020). Measuring and interpreting transposable element expression. Nature reviews. Genetics, 10.1038/s41576-020-0251-y. Advance online publication. 10.1038/s41576-020-0251-y
Lemaître, J. F., Ronget, V., Tidière, M., Allainé, D., Berger, V., Cohas, A., Colchero, F., Conde, D. A., Garratt, M., Liker, A., Marais, G., Scheuerlein, A., Székely, T., and Gaillard, J. M. (2020). Sex differences in adult lifespan and aging rates of mortality across wild mammals. Proceedings of the National Academy of Sciences of the United States of America, 117(15), 8546–8553. 10.1073/pnas.1911999117
Lemos, B., Araripe, L. O., and Hartl, D. L. (2008). Polymorphic Y chromosomes harbor cryptic variation with manifold functional consequences. Science (New York, N.Y.), 319(5859), 91–93. 10.1126/science.1148861
Lerat, E., Fablet, M., Modolo, L., Lopez-Maestre, H., and Vieira, C. (2017). TEtools facilitates big data expression analysis of transposable elements and reveals an antagonism between their activity and that of piRNA genes. Nucleic acids research, 45(4), e17. 10.1093/nar/gkw953
Marais, G., Gaillard, J. M., Vieira, C., Plotton, I., Sanlaville, D., Gueyffier, F., and Lemaitre, J. F. (2018). Sex gap in aging and longevity: can sex chromosomes play a role?. Biology of sex differences, 9(1), 33. 10.1186/s13293-018-0181-y
Milot, E., Moreau, C., Gagnon, A., Cohen, A. A., Brais, B., and Labuda, D. (2017). Mother's curse neutralizes natural selection against a human genetic disease over three centuries. Nature ecology and evolution, 1(9), 1400–1406. 10.1038/s41559-017-0276-6
Pipoly, I., Bókony, V., Kirkpatrick, M., Donald, P. F., Székely, T., and Liker, A. (2015). The genetic sex-determination system predicts adult sex ratios in tetrapods. Nature, 527(7576), 91–94. 10.1038/nature15380
Tidière, M., Gaillard, J. M., Müller, D. W., Lackey, L. B., Gimenez, O., Clauss, M., and Lemaître, J. F. (2015). Does sexual selection shape sex differences in longevity and senescence patterns across vertebrates? A review and new insights from captive ruminants. Evolution; international journal of organic evolution, 69(12), 3123–3140. 10.1111/evo.12801
Xirocostas, Z. A., Everingham, S. E., and Moles, A. T. (2020). The sex with the reduced sex chromosome dies earlier: a comparison across the tree of life. Biology letters, 16(3), 20190867. 10.1098/rsbl.2019.0867

Two evolutionary processes have been shown in theory to enhance the effects of natural selection in purging deleterious mutations from a population (here ""natural"" selection is defined as ""selection other than sexual selection""). First, inbreeding, especially self-fertilization, facilitates the removal of deleterious recessive alleles, the effects of which are largely hidden from selection in heterozygotes when mating is random. Second, sexual selection can facilitate the removal of deleterious alleles of arbitrary dominance, with little or no demographic cost, provided that deleterious effects are greater in males than in females (""genic capture""). Inbreeding (especially selfing) and sexual selection are often negatively correlated in nature. Empirical tests of the role of sexual selection in purging deleterious mutations have been inconsistent, potentially due to the positive relationship between sexual selection and intersexual genetic conflict.
In their preprint, Noël et al. [1] report a cleverly designed, and impressively long-term, experimental evolution study designed to tease apart the relative contributions of selfing and sexual selection in purging deleterious mutations, using the self-compatible hermaphroditic snail Physa acuta. Hermaphroditism relieves at least some of the potential conflict between males and females because each individual expresses traits of each sex. The authors report a 50-generation (ten years!) evolution experiment with four experimental treatments: Control (C), in which snails reproduced by mass mating (allowing sexual selection) and the next generation was sampled randomly from offspring in proportion to maternal family size; Male-selection (M) in which snails reproduced by mass mating but maternal family size was held constant, removing the opportunity for fertility selection; Female fertility selection (F) in which snails mated monogamously but fertility selection was imposed, and selfing (S), in which snails reproduced by selfing every other generation, alternating with monogamy + fertility selection. Juvenile survival was taken as the proxy for fitness and was measured for offspring of self-fertilization and of outcross matings. Each line type (C, M, F, S) was replicated twice.
The results are enviably clear-cut: after 50 generations of evolution, outcross fitness dropped precipitously in the F treatment (monogamy+female fertility selection) and remained at ancestral levels in the other three treatments. Clearly, sexual selection in males is more efficient at purging deleterious alleles than is female fertility selection. Similarly, inbreeding depression was reduced in the S lines relative to the other treatments, indicating that, unsurprisingly, deleterious recessive mutations of large effect are purged under strong inbreeding. Outcross fitness in the S lines did not decline, in contrast to the F lines, which indicates that deleterious mutations are on average slightly recessive.
Taken as a whole, this study by Noël et al. [1] provides a compelling empirical demonstration of the efficacy of both sexual selection and strong inbreeding as mechanisms of purging, and implicates sexual conflict as a potentially important factor in studies in which relaxation of sexual selection fails to result in purging.

References

[1] Noël, E., Fruitet, E., Lelaurin, D., Bonel, N., Segard, A., Sarda, V., Jarne, P., & David P. (2018). Sexual selection and inbreeding: two efficient ways to limit the accumulation of deleterious mutations. bioRxiv, 273367, ver. 3 recommended and peer-reviewed by PCI Evol Biol. doi: 10.1101/273367

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

Ecological specialisation, especially among parasites infecting a set of host species, is ubiquitous in nature. Host specialisation can be understood as resulting from trade-offs in parasite infectivity, virulence and growth. However, it is not well understood how variation in these trade-offs shapes the overall fitness trade-off a parasite faces when adapting to multiple hosts. For instance, it is not clear whether a strong trade-off in one fitness component may sufficiently constrain the evolution of a generalist parasite despite weak trade-offs in other components. A second mechanism explaining variation in specialisation among species is habitat availability and quality. Rare habitats or habitats that act as ecological sinks will not allow a species to persist and adapt, preventing a generalist phenotype to evolve. Understanding the prevalence of those mechanisms in natural systems is crucial to understand the emergence and maintenance of host specialisation, and biodiversity in general.
In their study "Trait-specific trade-offs prevent niche expansion in two parasites", Lievens et al. [1] report the results of an evolution experiment involving two parasitic microsporidians, Anostracospora rigaudi and Enterocytospora artemiae, infecting two sympatric species of brine shrimp, Artemia franciscana and Artemia parthenogenetica. The two parasites were originally specialised on their primary host: A. rigaudi on A. parthenogenetica and E. artemiae on A. franciscana, although they encounter both species in the wild but at different rates. After passaging each parasite on each single host and on both hosts alternatively, Lievens et al. asked how host specialisation evolved. They found no change in specialisation at the fitness level in A. rigaudi in either treatment, while E. artemiae became more of a generalist after having been exposed to its secondary host, A. parthenogenetica. The most interesting part of the study is the decomposition of the fitness trade-off into its underlying trade-offs in spore production, infectivity and virulence. Both species remained specialised for spore production on their primary host, interpreted as caused by a strong trade-off between hosts preventing improvements on the secondary host. A. rigaudi evolved reduced virulence on its primary host without changes in the overall fitness trad-off, while E. artemiae evolved higher infectivity on its secondary host making it a more generalist parasite and revealing a weak trade-off for this trait and for fitness. Nevertheless, both parasites retained higher fitness on their primary host because of the lack of an evolutionary response in spore production.
This study made two important points. First, it showed that despite apparent strong trade-off in spore production, a weak trade-off in infectivity allowed E. artemiae to become less specialised. In contrast, A. rigaudi remained specialised, presumably because the strong trade-off in spore production was the overriding factor. The fitness trade-off that results from the superposition of multiple underlying trade-offs is thus difficult to predict, yet crucial to understand potential evolutionary outcomes. A second insight is related to the ecological context of the evolution of specialisation. The results showed that E. artemiae should be less specialised than observed, which points to a role played by source-sink dynamics on A. parthenogenetica in the wild. The experimental approach of Lievens et al. thus allowed them to nicely disentangle the various sources of constraints on the evolution of host adaptation in the Artemia system.

References

[1] Lievens, E.J.P., Michalakis, Y. and Lenormand, T. (2019). Trait-specific trade-offs prevent niche expansion in two parasites. bioRxiv, 621581, ver. 4 peer-reviewed and recommended by PCI Evolutionary Biology. doi: 10.1101/621581

Parasitoid wasps have developed different mechanisms to increase their parasitic success, usually at the expense of host survival (Fellowes and Godfray, 2000). Eggs of these insects are deposited inside the juvenile stages of their hosts, which in turn deploy several immune response strategies to eliminate or disable them (Yang et al., 2020). Drosophila melanogaster protects itself against parasitoid attacks through the production of specific elongated haemocytes called lamellocytes which form a capsule around the invading parasite (Lavine and Strand, 2002; Rizki and Rizki, 1992) and the subsequent activation of the phenol-oxidase cascade leading to the release of toxic radicals (Nappi et al., 1995). On the parasitoid side, robust responses have evolved to evade host immune defenses as for example the Drosophila-specific endoparasite Leptopilina boulardi, which releases venom during oviposition that modifies host behaviour (Varaldi et al., 2006) and inhibits encapsulation (Gueguen et al., 2011; Martinez et al., 2012).
Studies have shown that the wasp parasitic capacity is correlated to venom presence and its content (Colinet et al., 2009; Poirié et al., 2014), including that evolution of venom protein composition is driven by different levels of host susceptibility to infection (Cavigliasso et al., 2019). However, it had not been determined to this day, if and how parasitic range can affect venom protein composition and to which extent host specialization requires broad-spectrum factors or a plethora of specialized components.
These outstanding questions are now approached in a study by Cavigliasso and colleagues (Cavigliasso et al., 2021), where they perform experimental evolution of L. boulardi for 9 generations exposing it to different Drosophila host species and genetic backgrounds (two strains of D. melanogaster, D. simulans and D. yakuba). The authors tested whether the parasitic success of each selection regime was host-specific and how they influenced venom composition in parasitoids. For the first part, infection outcomes were assayed for each selection regime when cross-infecting different hosts. To get a finer measurement of the mechanisms under selection, the authors differentiated three phenotypes: overall parasitic success, encapsulation inhibition and escape from capsule. Throughout the course of experimental evolution, only encapsulation inhibition did not show an improved response upon selection on any host. Importantly, the cross-infection scenario revealed a clear specificity to the selected host for each evolved resistance.
As for venom composition, a trend of differential evolution was detected between host species, although a significant part of that was due to a larger differentiation in the D. yakuba regime, which showed a completely different directionality. Importantly, the authors could identify some of the specific proteins targeted by the several selection regimes, whether selected or counter-selected for. Interestingly, the D. yakuba regime is the only case where the key parasitoid protein LbSPNy (Colinet et al., 2009) was not counter-selected and the only regime in which the overall venom composition did not evolve towards the Ism strain, one of the two ancestral strains of L. boulardi used in the study. It is possible that these two results are correlated, since LbSPNy has been described to inhibit activation of the phenoloxidase cascade in D. yakuba and is one of the most abundant proteins in the ISy venom, making it a good target for selection (Colinet et al., 2013). The authors also discuss the possibility that this difference is related to the geographical distribution of the strains of L. boulardi, since each coincide with either D. melanogaster or D. yakuba.
This methodologically broad work by Cavigliasso and colleagues constitutes an important experimental contribution towards the understanding of how parasitoid adaptation to specific hosts is achieved at different phenotypic and mechanistic levels. It provides compelling evidence that venom composition evolves differently in response to specific parasitic ranges, particularly considering the evolutionary difference between the selective hosts. In line with this result, it is also concluded that the majority of venom proteins selected are lineage-specific, although a few broad-spectrum factors could also be detected. 
The question of whether parasitic range can affect venom composition and parasitic success is still open to more contributions. A potentially interesting long-term direction will be to use a similar setup of experimental evolution on the generalist L. heterotoma (Schlenke et al., 2007) . On a more immediate horizon, comparing the venom evolution of both L. heterotoma and L. boulardi under selection with different hosts and under cross-infection scenarios could reveal interesting patterns. The recent sequencing of the L. boulardi genome together with the vast number of studies addressing mechanisms of Drosophila resistance to parasitoid infection, will enable the thorough characterization of the genetic basis of host-parasitoid interactions and the deeper understanding of these ubiquitous and economically-relevant relationships.
 
*This recommendation text has been co-written with Tânia F. Paulo who is not a recommender of PCI Evol Biol

References

Cavigliasso, F., Mathé-Hubert, H., Gatti, J.-L., Colinet, D. and Poirié, M. (2021) Parasitic success and venom composition evolve upon specialization of parasitoid wasps to different host species. bioRxiv, 2020.10.24.353417, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2020.10.24.353417

Cavigliasso, F., Mathé-Hubert, H., Kremmer, L., Rebuf, C., Gatti, J.-L., Malausa, T., Colinet, D., Poiré, M. and  Léne. (2019). Rapid and Differential Evolution of the Venom Composition of a Parasitoid Wasp Depending on the Host Strain. Toxins, 11(629). https://doi.org/10.3390/toxins11110629

Colinet, D., Deleury, E., Anselme, C., Cazes, D., Poulain, J., Azema-Dossat, C., Belghazi, M., Gatti, J. L. and  Poirié, M. (2013). Extensive inter- and intraspecific venom variation in closely related parasites targeting the same host: The case of Leptopilina parasitoids of Drosophila. Insect Biochemistry and Molecular Biology, 43(7), 601–611. https://doi.org/10.1016/j.ibmb.2013.03.010

Colinet, D., Dubuffet, A., Cazes, D., Moreau, S., Drezen, J. M. and  Poirié, M. (2009). A serpin from the parasitoid wasp Leptopilina boulardi targets the Drosophila phenoloxidase cascade. Developmental and Comparative Immunology, 33(5), 681–689. https://doi.org/10.1016/j.dci.2008.11.013

Fellowes, M. D. E. and  Godfray, H. C. J. (2000). The evolutionary ecology of resistance to parasitoids by Drosophila. Heredity, 84(1), 1–8. https://doi.org/10.1046/j.1365-2540.2000.00685.x

Gueguen, G., Rajwani, R., Paddibhatla, I., Morales, J. and  Govind, S. (2011). VLPs of Leptopilina boulardi share biogenesis and overall stellate morphology with VLPs of the heterotoma clade. Virus Research, 160(1–2), 159–165. https://doi.org/10.1016/j.virusres.2011.06.005

Lavine, M. D. and  Strand, M. R. (2002). Insect hemocytes and their role in immunity. Insect Biochemistry and Molecular Biology, 32(10), 1295–1309. https://doi.org/10.1016/S0965-1748(02)00092-9

Martinez, J., Duplouy, A., Woolfit, M., Vavre, F., O’Neill, S. L. and  Varaldi, J. (2012). Influence of the virus LbFV and of Wolbachia in a host-parasitoid interaction. PloS One, 7(4), e35081. https://doi.org/10.1371/journal.pone.0035081

Nappi, A. J., Vass, E., Frey, F. and  Carton, Y. (1995). Superoxide anion generation in Drosophila during melanotic encapsulation of parasites. European Journal of Cell Biology, 68(4), 450–456.

Poirié, M., Colinet, D. and  Gatti, J. L. (2014). Insights into function and evolution of parasitoid wasp venoms. Current Opinion in Insect Science, 6, 52–60. https://doi.org/10.1016/j.cois.2014.10.004

Rizki, T. M. and  Rizki, R. M. (1992). Lamellocyte differentiation in Drosophila larvae parasitized by Leptopilina. Developmental and Comparative Immunology, 16(2–3), 103–110. https://doi.org/10.1016/0145-305X(92)90011-Z

Schlenke, T. A., Morales, J., Govind, S. and  Clark, A. G. (2007). Contrasting infection strategies in generalist and specialist wasp parasitoids of Drosophila melanogaster. PLoS Pathogens, 3(10), 1486–1501. https://doi.org/10.1371/journal.ppat.0030158

Varaldi, J., Petit, S., Boulétreau, M. and  Fleury, F. (2006). The virus infecting the parasitoid Leptopilina boulardi exerts a specific action on superparasitism behaviour. Parasitology, 132(Pt 6), 747–756. https://doi.org/10.1017/S0031182006009930

Yang, L., Qiu, L., Fang, Q., Stanley, D. W. and  Gong‐Yin, Y. (2020). Cellular and humoral immune interactions between Drosophila and its parasitoids. Insect Science. https://doi.org/10.1111/1744-7917.12863