Biotic interactions are often shaped by abiotic factors (Liu and Gaines 2022). Although this notion is not new in ecology and evolutionary biology, we are still far from a thorough understanding of how biotic interactions change along abiotic gradients in space and time. This is particularly challenging because abiotic factors can affect organisms and their interactions in multiple – direct or indirect – ways. For example, because abiotic conditions strongly determine how energy enters biological systems via producers, their effects can propagate through entire food webs, from the bottom to the top (O’Connor 2009, Gilbert et al 2019). Understanding how biological diversity - both within and across species - is shaped by the indirect effects of environmental conditions is a timely question as climate change and anthropogenic activities have been altering temperature and water availability across different ecosystems.

Motivated by the current water crisis and severe droughts predicted for the near future worldwide (du Plessis 2019), Migeon et al. (2023) investigated how water limitation on producers scales up to affect life-history patterns of a widespread crop pest, the spider mite Tetranychus urticae. The authors sampled spider mite populations (n = 12) along a striking gradient of climatic conditions (>16 degrees of latitude) in Europe. After letting mites acclimate to lab conditions for several generations, the authors performed a common garden experiment to quantify how the life-history traits of mite populations from different locations respond to drought stress in their host plants.

Curiously, the authors found that, when reared on drought-stressed plants, mites tended to develop faster, had higher fecundity and lower dispersion rates. This response was in line with some results obtained previously with Tetranychus species (e.g. Ximénez-Embun et al 2016). Importantly, despite some experimental caveats in the experimental design, which makes it difficult to completely disentangle the specific effects of location vs. environmental noise, results suggest the climate that populations originally experienced was also an important determinant of the plastic response in these herbivores. In fact, populations from wetter and colder regions showed a steeper change in drought response, while populations from arid climates showed a shallower response. This interesting result suggests the importance of intraspecific (between-populations) variation in the response to drought, which might be explained by the climatic heterogeneity in space throughout the evolutionary history of different populations. These results become even more important in our rapidly changing world, highlighting the importance of considering genetic variation (and conditions that generate it) when predicting plastic and evolutionary responses to stressful conditions.
 
REFERENCES

du Plessis, A. (2019). Current and Future Water Scarcity and Stress. In: Water as an Inescapable Risk. Springer Water. Springer, Cham. https://doi.org/10.1007/978-3-030-03186-2
 
Gibert, J.P. Temperature directly and indirectly influences food web structure. Sci Rep 9, 5312 (2019). https://doi.org/10.1038/s41598-019-41783-0
 
Liu, O. R., & Gaines, S. D. (2022). Environmental context dependency in species interactions. Proceedings of the National Academy of Sciences, 119(36), e2118539119. https://doi.org/10.1073/pnas.2118539119
 
Migeon A., Auger P., Fossati-Gaschignard O., Hufbauer R.A, Miranda M., Zriki G., Navajas M. (2023) The response to drought-stressed host plants varies among herbivorous mite populations from a climate gradient. bioRxiv, 2021.10.21.465244, ver. 4 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2021.10.21.465244
 
O'Connor, M.I. (2009), Warming strengthens an herbivore-plant interaction. Ecology, 90: 388-398. https://doi.org/10.1890/08-0034.1
 
Ximénez-Embún, M. G., Ortego, F., & Castañera, P. (2016). Drought-stressed tomato plants trigger bottom-up effects on the invasive Tetranychus evansi. PloS one, 11(1), e0145275. https://doi.org/10.1371/journal.pone.0145275

Until now, very little is known about the tail use and functional performance in tail prehensile animals. Luger et al. (2020) are the first to provide explorative observations on trait related modulation of tail use, despite the lack of a sufficiently standardized data set to allow statistical testing. They described whether gap distance, perch diameter, and perch roughness influence tail use and overall locomotor behavior of the species Chamaeleo calyptratus.
Peterson (1984) described already the pattern how and when the tail is moved when bridging the distance from one perch to another. The study by Luger et al. (2020) further explores how this bridging distance, as well as other perch parameters modulate this behavior and the importance of tail use in it. Zippel et al. (1999) study the underlying musculoskeletal anatomy of the tail in chameleons, showing that chameleons have a strikingly different tail anatomy than other prehensile squamates. The difference is (partially) to be seen in the capacity of tail autotomy, that has been lost in chameleons.
Luger et al. (2020) describe the role the tail has in bridging a gap, and show that challenging and acrobatic movements to bridge large gaps, or when grasping on not so rough surfaces, relies heavily on a strong tail. Full body suspension with the tail can explain why tail autotomy has been lost, thus explaining the diverging tail musculature. They speculate on the role of this behavior for sexual selection for males. Sexual selection for males with a higher gripping performance could explain why male chameleons perform better for their size. In addition, boldness could have played a role. The authors state that exploring personality and its links to morphology, performance, and behaviors like grap-bridging would be a worthwhile avenue for future research on sexual selection in reptiles.

References

Luger, A.M., Vermeylen, V., Herrel, A. and Adriaens, D. (2020) Do substrate roughness and gap distance impact gap-bridging strategies in arboreal chameleons? bioRxiv, 2020.08.21.260596, ver. 3 peer-reviewed and recommended by PCI Zoology. doi: https://doi.org/10.1101/2020.08.21.260596
Peterson, J. A. (1984). The locomotion of Chamaeleo (Reptilia: Sauria) with particular reference to the forelimb. Journal of Zoology, 202(1), 1-42. doi: https://doi.org/10.1111/j.1469-7998.1984.tb04286.x
Zippel, K. C., Glor, R. E., and Bertram, J. E. (1999). On caudal prehensility and phylogenetic constraint in lizards: the influence of ancestral anatomy on function in Corucia and Furcifer. Journal of Morphology, 239(2), 143-155. doi: https://doi.org/10.1002/(SICI)1097-4687(199902)239:2%3C143::AID-JMOR3%3E3.0.CO;2-O

Medical and veterinary entomology is a discipline that deals with the role of insects on human and animal health. A primary objective is the identification of vectors that transmit pathogens. This is the aim of Beranek and co-authors in their study [1]. They focus on mosquito vector species responsible for transmission of St. Louis encephalitis virus (SLEV), an arbovirus that circulates in avian species but can incidentally occur in dead end mammal hosts such as humans, inducing symptoms and sometimes fatalities. Culex pipiens quinquefasciatus is known as the most common vector, but other species are suspected to also participate in transmission. Among them Culex saltanensis and Culex interfor have been found to be infected by the virus in the context of outbreaks. The fact that field collected mosquitoes carry virus particles is not evidence for their vector competence: indeed to be a competent vector, the mosquito must not only carry the virus, but also the virus must be able to replicate within the vector, overcome multiple barriers (until the salivary glands) and be present at sufficient titre within the saliva. This paper describes the experiments implemented to evaluate the vector competence of Cx. saltanensis and Cx. interfor from ingestion of SLEV to release within the saliva. Females emerged from field-collected eggs of Cx. pipiens quinquefasciatus, Cx. saltanensis and Cx. interfor were allowed to feed on SLEV infected chicks and viral development was measured by using (i) the infection rate (presence/absence of virus in the mosquito abdomen), (ii) the dissemination rate (presence/absence of virus in mosquito legs), and (iii) the transmission rate (presence/absence of virus in mosquito saliva). The sample size for each species is limited because of difficulties for collecting, feeding and maintaining large numbers of individuals from field populations, however the results are sufficient to show that this strain of SLEV is able to disseminate and be expelled in the saliva of mosquitoes of the three species at similar viral loads. This work therefore provides evidence that Cx saltanensis and Cx interfor are competent species for SLEV to complete its life-cycle. Vector competence does not directly correlate with the ability to transmit in real life as the actual vectorial capacity also depends on the contact between the infectious vertebrate hosts, the mosquito life expectancy and the extrinsic incubation period of the viruses. The present study does not deal with these characteristics, which remain to be investigated to complete the picture of the role of Cx saltanensis and Cx interfor in SLEV transmission. However, this study provides proof of principle that that SLEV can complete it’s life-cycle in Cx saltanensis and Cx interfor. Combined with previous knowledge on their feeding preference, this highlights their potential role as bridge vectors between birds and mammals. These results have important implications for epidemiological forecasting and disease management. Public health strategies should consider the diversity of vectors in surveillance and control of SLEV.

References
[1] Beranek, M. D., Quaglia, A. I., Peralta, G. C., Flores, F. S., Stein, M., Diaz, L. A., Almirón, W. R. and Montigiani, M. S. (2020). Culex saltanensis and Culex interfor (Diptera: Culicidae) are susceptible and competent to transmit St. Louis encephalitis virus (Flavivirus: Flaviviridae) in central Argentina. bioRxiv 722579, ver. 6 peer-reviewed and recommended by PCI Entomology. doi: 10.1101/722579

Host-parasitoid interactions have been the focus of extensive ecological research for decades. One the of the major reasons is the importance host-parasitoid interactions play for the biological control of crop pests. Parasitoids are the main natural regulators for a large number of economically important pest insects, and in many cases they could be the only viable crop protection strategy. Parasitoids are also integral part of complex food webs whose structure and diversity display large spatio-temporal variations [1-3]. With the increasing globalization of human activities, the generalized spread and establishment of invasive species is a major cause of disruption in local community and food web spatio-temporal dynamics. In particular, the deliberate introduction of non-native parasitoids as part of biological control programs, aiming the suppression of established, and also highly invasive crop pests, is a common practice with potentially significant, yet poorly understood effects on local food web dynamics (e.g. [4]).
In their study, Muru et al. [5] took advantage of an existing biological control program focusing on the Asian chestnut gall wasp Dryocosmus kuriphilus, an invasive (and highly damaging) pest of chestnut trees. The species is currently a successful invader in many geographic regions, including southern France, where local parasitoid communities failed to provide an adequate control since its widespread establishment in 2010 [6]. In response, the non-native parasitoid species Torymus sinensis, which is highly-specific to the Asian chestnut gall wasp, was massively released in commercial chestnut orchards across several regions in France and the island of Corsica. The pest population outbreak was successfully contained, and thanks to the vast amount of host-parasitoid interaction data collected as part of the program, the authors were able to explore the effects of the large fluctuations in Asian chestnut gall wasp natural abundances on native parasitoid communities, immediately before, and up to five years following the introduction of its natural enemy T. sinensis.
Using co-occurrence and clustering analyses, Muru et al. [5] demonstrate that the invasion and the consecutive (efficient) control of the Asian chestnut gall wasp by the parasitoid T. sinensis have a significant impact on the structure of local parasitoid food webs. In particular, following decline in the Asian chestnut gall wasp’s populations, native parasitoids markedly switched to alternative hosts, most likely due to their respectively higher relative abundances. This pattern seemed to be driven by the degree of generalism in native parasitoid species. Indeed, when its abundances were still relatively high, the Asian chestnut gall wasp was primarily attacked by species capable of exploiting a broad range of hosts, while at low population densities only specialist parasitoids such as Mesolobus sericeus were able to persist and compete with the non-native T. sinensis.
The current study is important for two major reasons. First, it underscores the value of long-term species interaction data in order to understand the dynamic nature of food webs, namely their structural flexibility in response to changes in the environment or, as in this case, large fluctuation in abundances of a major pest species. In this context, biological control programs could be a great source of data for exploring long-term, large-scale dynamics of species interactions, and their use in ecological studies deserves to be further emphasized. Second, the study adds to the increasing empirical evidence that mobile generalist foragers can display adaptive, frequency-dependent switching behaviour ([1], [7]), which has been suggested to act as a key stabilizing mechanism in food webs by buffering fluctuating population dynamics at larger spatial scales ([8- 10]).
However, the timing of such buffering seems important, especially in systems such as commercial chestnut orchards. Despite their capacity to adaptively switch their foraging behaviour, the response of the native parasitoid communities to the new, unfamiliar resource was not fast enough in order to contain the primary outbreak under an appropriate damage threshold, thus requiring the introduction of the more specialized parasitoid T. sinensis. Nevertheless, based on current ecological theory, results presented by Muru et al. [5] suggest that the response of native parasitoid community to fluctuating host dynamics – i.e. shifts in parasitoid foraging behaviour based on their traits – could be predictable. This is encouraging considering the growing impact of biological invasions and insect pest outbreaks, but also the need to implement efficient, yet sustainable strategies for crop protection. Future studies would show at what extent observations by Muru et al. [5] are generalizable over longer time periods or other model systems. Noticeably, better understanding about population dynamics and interactions with the broader community of hosts available across habitats should allow to fine-tune predictions about parasitoids’ response to fluctuating resources.

References

[1] Eveleigh ES, McCann KS, McCarthy PC, Pollock SJ, Lucarotti CJ, Morin B, McDougall GA, Strongman DB, Huber JT, Umbanhowar J, Faria LDB (2007). Fluctuations in density of an outbreak species drive diversity cascades in food webs. Proc. Natl. Acad. Sci. USA 104, 16976-16981. doi: 10.1073/pnas.0704301104
[2] Tylianakis JM, Tscharntke T, Lewis OT (2007). Habitat modification alters the structure of tropical host–parasitoid food webs. Nature 445, 202-205. doi: 10.1038/nature05429
[3] Murakami M, Hirao T, Kasei A (2008). Effects of habitat configuration on host–parasitoid food web structure. Ecol. Res. 23, 1039-1049. doi: 10.1007/s11284-008-0478-0
[4] Geslin B, Gauzens B, Baude M, Dajoz I, Fontaine C, Henry M, Ropars L, Rollin O, Thébault E, Vereecken NJ (2016). Massively introduced managed species and their consequences for plant–pollinator interactions. Adv. Ecol. Res. 57, 147-199. doi: 10.1016/bs.aecr.2016.10.007
[5] Muru D, Borowiec N, Thaon M, Ris N, Viciriuc M I, Warot S, Vercken E (2020) The open bar is closed: restructuration of a native parasitoid community following successful control of an invasive pest. bioRxiv, 2019.12.20.884908, ver. 6 peer-reviewed and recommended by PCI Zoology. doi: 10.1101/2019.12.20.884908
[6] Borowiec N, Thaon M, Brancaccio L, Warot S, Vercken E, Fauvergue X, Ris N, Malausa J-C (2014). Classical biological control against the chestnut gall wasp 'Dryocosmus kuriphilus' (Hymenoptera, Cynipidae) in France. Plant Prot. Q. 29, 7-10.
[7] Bartley TJ, McCann KS, Bieg C, Cazelles K, Granados M, Guzzo MM, MacDougall AS, Tunney TD, McMeans BC (2019). Food web rewiring in a changing world. Nat. Ecol. Evol. 3, 345–354. doi: 10.1038/s41559-018-0772-3
[8] Kondoh M (2003). Foraging adaptation and the relationship between food-web complexity and stability. Science. 299, 1388-1391. doi: 10.1126/science.1079154
[9] McCann KS, Rooney N (2009). The more food webs change, the more they stay the same. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 1789-801. doi: 10.1098/rstb.2008.0273
[10] Valdovinos FS, Ramos-Jiliberto R, garay-Narváez L, Urbani P, Dunne JA (2010). Consequences of adaptive behaviour for the structure and dynamics of food webs. Ecol. Lett. 13, 1546-1559. doi: 10.1111/j.1461-0248.2010.01535.x

Polyphenisms offer an opportunity to study the links between phenotype, development, and environment in a controlled genomic context (Simpson, Sword, & Lo, 2011). In organisms with short generation times, individuals living and developing in different seasons encounter different environmental conditions. Adaptive plasticity allows them to express different phenotypes in response to seasonal cues, such as temperature or photoperiod. Such phenotypes can be morphological variants, for instance displaying different wing patterns as seen in butterflies (Brakefield & Larsen, 1984; Nijhout, 1991; Windig, 1999), or physiological variants, characterized for instance by direct development vs winter diapause in temperate insects (Dalin & Nylin, 2012; Lindestad, Wheat, Nylin, & Gotthard, 2019; Shearer et al., 2016). 

Many aphids display cyclical parthenogenesis, a remarkable seasonal polyphenism for reproductive mode (Tagu, Sabater-Muñoz, & Simon, 2005), also sometimes coupled with wing polyphenism (Braendle, Friebe, Caillaud, & Stern, 2005), which allows them to switch between parthenogenesis during spring and summer to sexual reproduction and the production of diapausing eggs before winter. In the pea aphid Acyrthosiphon pisum, photoperiod shortening results in the production, by parthenogenetic females, of embryos developing into the parthenogenetic mothers of sexual individuals. The link between parthenogenetic reproduction and sexual reproduction, therefore, occurs over two generations, changing from a parthenogenetic form producing parthenogenetic females (virginoparae), to a parthenogenetic form producing sexual offspring (sexuparae), and finally sexual forms producing overwintering eggs (Le Trionnaire et al., 2022).  

The molecular basis for the transduction of the environmental signal into reproductive changes is still unknown, but the dopamine pathway is an interesting candidate. Form-specific expression of certain genes in the dopamine pathway occurs downstream of the perception of the seasonal cue, notably with a marked decrease in the heads of embryos reared under short-day conditions and destined to become sexuparae. Dopamine has multiple roles during development, with one mode of action in cuticle melanization and sclerotization, and a neurological role as a synaptic neurotransmitter. Both modes of action might be envisioned to contribute functionally to the perception and transduction of environmental signals. 

In this study, Le Trionnaire and colleagues aim at clarifying this role in the pea aphid (Le Trionnaire et al., 2022). Using quantitative RT-PCR, RNA-seq, and in situ hybridization of RNA probes, they surveyed the timing and spatial patterns of expression of dopamine pathway genes during the development of different stages of embryo to larvae reared under long and short-day conditions, and destined to become virginoparae or sexuparae females, respectively. The genes involved in the synaptic release of dopamine generally did not show differences in expression between photoperiodic treatments. By contrast, pale and ddc, two genes acting upstream of dopamine production, generally tended to show a downregulation in sexuparare embryo, as well as genes involved in cuticle development and interacting with the dopamine pathway. The downregulation of dopamine pathway genes observed in the heads of sexuparare juveniles is already detectable at the embryonic stage, suggesting embryos might be sensing environmental cues leading them to differentiate into sexuparae females.

The way pale and ddc expression differences could influence environmental sensitivity is still unclear. The results suggest that a cuticle phenotype specifically in the heads of larvae could be explored, perhaps in the form of a reduction in cuticle sclerotization and melanization which might allow photoperiod shortening to be perceived and act on development. Although its causality might be either way, such a link would be exciting to investigate, yet the existence of cuticle differences between the two reproductive types is still a hypothesis to be tested. The lack of differences in the expression of synaptic release genes for dopamine might seem to indicate that the plastic response to photoperiod is not mediated via neurological roles. Yet, this does not rule out the role of decreasing levels of dopamine in mediating this response in the central nervous system of embryos, even if the genes regulating synaptic release are equally expressed. 

To test for a direct role of ddc in regulating the reproductive fate of embryos, the authors have generated CrispR-Cas9 knockout mutants. Those mutants displayed egg cuticle melanization, but with lethal effects, precluding testing the effect of ddc at later stages in development. Gene manipulation becomes feasible in the pea aphid, opening up certain avenues for understanding the roles of other genes during development.

This study adds nicely to our understanding of the intricate changes in gene expression involved in polyphenism. But it also shows the complexity of deciphering the links between environmental perception and changes in physiology, which mobilise multiple interacting gene networks. In the era of manipulative genetics, this study also stresses the importance of understanding the traits and phenotypes affected by individual genes, which now seems essential to piece the puzzle together.

References

Braendle C, Friebe I, Caillaud MC, Stern DL (2005) Genetic variation for an aphid wing polyphenism is genetically linked to a naturally occurring wing polymorphism. Proceedings of the Royal Society B: Biological Sciences, 272, 657–664. https://doi.org/10.1098/rspb.2004.2995

Brakefield PM, Larsen TB (1984) The evolutionary significance of dry and wet season forms in some tropical butterflies. Biological Journal of the Linnean Society, 22, 1–12. https://doi.org/10.1111/j.1095-8312.1984.tb00795.x

Dalin P, Nylin S (2012) Host-plant quality adaptively affects the diapause threshold: evidence from leaf beetles in willow plantations. Ecological Entomology, 37, 490–499. https://doi.org/10.1111/j.1365-2311.2012.01387.x

Le Trionnaire G, Hudaverdian S, Richard G, Tanguy S, Gleonnec F, Prunier-Leterme N, Gauthier J-P, Tagu D (2022) Dopamine pathway characterization during the reproductive mode switch in the pea aphid. bioRxiv, 2020.03.10.984989, ver. 4 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2020.03.10.984989

Lindestad O, Wheat CW, Nylin S, Gotthard K (2019) Local adaptation of photoperiodic plasticity maintains life cycle variation within latitudes in a butterfly. Ecology, 100, e02550. https://doi.org/10.1002/ecy.2550

Nijhout HF (1991). The development and evolution of butterfly wing patterns. Washington, DC: Smithsonian Institution Press.

Shearer PW, West JD, Walton VM, Brown PH, Svetec N, Chiu JC (2016) Seasonal cues induce phenotypic plasticity of Drosophila suzukii to enhance winter survival. BMC Ecology, 16, 11. https://doi.org/10.1186/s12898-016-0070-3

Simpson SJ, Sword GA, Lo N (2011) Polyphenism in Insects. Current Biology, 21, R738–R749. https://doi.org/10.1016/j.cub.2011.06.006

Tagu D, Sabater-Muñoz B, Simon J-C (2005) Deciphering reproductive polyphenism in aphids. Invertebrate Reproduction & Development, 48, 71–80. https://doi.org/10.1080/07924259.2005.9652172

Windig JJ (1999) Trade-offs between melanization, development time and adult size in Inachis io and Araschnia levana (Lepidoptera: Nymphalidae)? Heredity, 82, 57–68. https://doi.org/10.1038/sj.hdy.6884510