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

In pollinator insects, especially bees, foraging is almost exclusively performed by females due to the close linkage with brood care. They collect pollen as a protein- and lipid-rich food to feed developing larvae in solitary and social species. Bees take carbohydrate-rich nectar in small quantities to fuel their flight and carry the pollen load. To optimise the foraging flight, they tend to be flower constant, reducing the flower handling time and time among individual inflorescences (Goulson, 1999). Males of pollinator species might be found on flowers as well. As they do not collect any pollen for brood care, their foraging flights and visits to flowers might not be shaped by the selective forces that optimise the foraging flights of females. They might stay longer in individual flowers, take up nectar if needed, but might unintentionally carry pollen on their body surface (Wolf & Moritz, 2014).
 
Bumblebees are excellent pollinators (Goulson, 2010), and a few species are exploited commercially for their delivery of pollination services (Velthuis & van Doorn, 2006). However, a monophyletic group of socially parasitic species – cuckoo bumblebees – has evolved amongst the bumblebees, lacking a worker caste. Cuckoo bee gynes usurp nests of free-living bumblebees, kill the resident queen, and forces the host workers to rear their offspring consisting of gynes and males (Lhomme & Hines, 2019). The level of affected colonies in an area can be up to 42% (Erler & Lattorff, 2010).
 
The behaviour of the cuckoo bumblebees, especially that of the males, has been rarely studied. The present study by Fisogni et al. (2021) has targeted the flower-visiting behaviour of workers and males of free-living bumblebees and males of the cuckoo species. They used behavioural observations of flower-visiting insects on Gentiana lutea, a plant from south-eastern Europe with yellow flowers arranged in whorls. While all three groups of bees visited the same number of plants, males of both types visited more flowers within a whorl, but cuckoo males spent more time on flowers within a whorl and the whole plant than the free-living bumblebees.
 
The flower visits of bumblebee workers are optimised, aiming at collecting as much pollen as possible within a short time frame. This, in turn, has consequences for the pollination process by enhancing cross-pollination between different plants. By contrast, males and especially cuckoo bumblebee males, are not selected for an optimised foraging pattern. Instead, they spend more time on flowers, eventually resulting in higher levels of pollen transfer within a plant (geitonogamy), which might lead to reduced plant fitness. This is the first study to relate the foraging behaviour of cuckoo bumblebees to pollination and plant fitness.
 
References
 
Erler, S., & Lattorff, H. M. G. (2010). The degree of parasitism of the bumblebee (Bombus terrestris) by cuckoo bumblebees (Bombus (Psithyrus) vestalis). Insectes sociaux, 57(4), 371-377. https://doi.org/10.1007/s00040-010-0093-2
 
Fisogni, A., Bogo, G., Massol, F., Bortolotti, L., Galloni, M. (2021). Cuckoo male bumblebees perform slower and longer flower visits than free-living male and worker bumblebees. Zenodo, 10.5281/zenodo.4489066, ver. 1.2 peer-reviewed and recommended by PCI Zoology. https://doi.org/10.5281/zenodo.4489066
 
Goulson, D. (1999). Foraging strategies of insects for gathering nectar and pollen, and implications for plant ecology and evolution. Perspectives in plant ecology, evolution and systematics, 2(2), 185-209. https://doi.org/10.1078/1433-8319-00070
 
Goulson, D. (2010). Bumblebees. Behaviour, Ecology, and Conservation, 2nd edn. Oxford University Press, Oxford.
 
Lhomme, P., Hines, H. M. (2019). Ecology and evolution of cuckoo bumble bees. Annals of the Entomological Society of America, 112, 122-140. https://doi.org/10.1093/aesa/say031
 
Velthuis, H. H. W., van Doorn, A. (2006). A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie, 37, 421-451. https://doi.org/10.1051/apido:2006019
 
Wolf, S., Moritz, R. F. A. (2014). The pollination potential of free-foraging bumblebee (Bombus spp.) males (Hymenoptera. Apidae). Apidologie, 45, 440-450. https://doi.org/10.1007/s13592-013-0259-9

Using entomopathogenic fungi for biological control is an effective method for controlling certain crop pests, with the perspective of reducing the use of chemical pesticides. Yet, the efficiency of pathogenic fungi is dependent upon many factors that need to be evaluated to improve biological control potential in the fields (Lacey, 2001). The article by Chailleux et al. (2024) presents an exciting contribution to the field of biological pest control, specifically focusing on using entomopathogenic fungi to manage the oriental fruit fly, Bactrocera dorsalis. This fly, a member of the Tephritidae family, is a major threat to orchards in Asia, the Pacific and Africa, as it attacks fruit and causes considerable damage, in addition to having a relatively rapid biological invasion dynamic (Clarke et al. 2005). 

The objective of the Chailleux et al. (2024) study was to evaluate the virulence of Metarhizium anisopliae spores (strain Met69) on B. dorsalis adult flies according to various conditions: the inoculation dose and spore load, the formulation (adjuvant) and temperature conditions. The focus on host specificity and on-target applications was conducted to ensure minimal impact on non-target organisms, which is crucial for sustainable agriculture. The main challenge in this system was to achieve high strain virulence to kill wild individuals with a low number of spores—therefore limiting impact on non-target species such as natural enemies—but with a sufficient incubation period to allow transmission from mass-reared insects to wild conspecifics (Leite et al. 2022). A comparison of different inoculation methods is also provided and is interesting from a methodological point of view for future studies or even large-scale applications.

Using a well-designed experimental setup, the authors show that high pathogenicity (measured by LD50) is achievable even at low spore doses and independently of the fly's sex. Lethal action speed was, however, dependent on the dose. Regarding temperature, the authors demonstrated that mycelium growth was affected by the mean temperature but, most importantly, by daily fluctuation regimes; night and day temperature alternation allowed faster growth than constant temperature. These notions of thermal fluctuations are still under-researched in terms of their modulating role in biological control yet seem central to understanding them, as the authors demonstrate here. The correlation between increased virulence and specific abiotic factors, such as temperature, offers valuable additional insights into the bioecology of the insect host and the fungal pathogen. Chailleux et al. finally point out the need for careful selection of adjuvants in formulations and pay attention to interactions with the abiotic environment to avoid compromising the effectiveness of biological control agents. Indeed, the survival rate of inoculated flies increased in the presence of the corn starch adjuvant, but this effect decreased with temperature. As corn starch unexpectedly delayed mortality, the authors suggest a potential for enhancing conspecific transmission

From a broader perspective, the study emphasizes the importance of standardizing virulence evaluation to optimize biological control strategies like auto-dissemination or vectoring with sterile males, particularly in field conditions. The study contributions are timely and essential for advancing sustainable pest management strategies and improving inoculation methods. The findings underscore the need for field trials to refine these strategies, particularly in Africa, where climatic factors may affect pathogen efficacy and fly behavior. I recommend publishing this article in a referenced journal like the Peer Community Journal. 

References

Chailleux, A. Coulibaly, ON, Diouf B, Diop S, Sohel A, Brevault T (2023) Dose, temperature and formulation shape Metarhizium anisopliae virulence against the oriental fruit fly: lessons for improving on-target control strategies. bioRxiv, ver.2 peer-reviewed and recommended by PCI Zoology https://doi.org/10.1101/2023.12.14.571642

Clarke, A. R. et al. (2005). Invasive phytophagous pests arising through a recent tropical evolutionary radiation: the Bactrocera dorsalis complex of fruit flies. Annu. Rev. Entomol., 50, 293-319. https://doi.org/10.1146/annurev.ento.50.071803.130428

Lacey, L. A. (2001). Formulation of microbial biopesticides: beneficial microorganisms, nematodes and seed treatments. J Invertebr Pathol, 77, 147. https://doi.org/10.1006/jipa.2000.5005

Leite, M. O. et al. (2022). Laboratory risk assessment of three entomopathogenic fungi used for pest control toward social bee pollinators. Microorganisms, 10, 1800. https://doi.org/10.3390/microorganisms10091800

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

The sorting of organisms along a fast-slow continuum through correlations between life history traits is a long-standing framework (Stearns 1983) and corresponds to the pace-of-life axis. This axis represents the variation in a continuum of life-history strategies, from fast-reproducing short-lived species to slow-reproducing long-lived species. The pace-of-life axis has been the focus of much research largely in mammals, birds, reptiles and plants but less so in invertebrates (Salguero-Gómez et al. 2016; Araya-Ajoy et al. 2018; Healy et al. 2019; Bakewell et al. 2020). Outcomes from this research have highlighted variation across taxa on this axis and mixed support for, and against, patterns expected of the pace-of-life continuum. Given this, a greater understanding of the variation of the pace-of-life across-, and within, taxa are needed. Indeed, Guicharnard et al. (2023) highlight several points regarding our broader understanding of pace-of-life. In general, invertebrates are poorly represented, the variation of pace-of-life across taxonomic scales is less well understood and the relationship between pace-of-life and dispersal, a key life history, requires more attention. Here, Guicharnard et al. (2023) provide a first attempt at addressing the relationship between dispersal and pace-of-life at different scales.

The authors, under controlled conditions, investigated how life-history traits and effective dispersal covary for 28 lines from five species of endoparasitoid wasps from the genus Trichogramma. At the species level negative correlations were found between development time and fecundity, matching pace-of-life axis predictions. Although this correlation was not found to be significant among lines, within species, a similar pattern of a negative correlation was observed. This outcome matches previous findings that consistent pace-of-life axes become more difficult to find at lower taxonomic levels. Unlike the other life-history traits measured, effective dispersal showed no evidence of differences between species or between lines. The authors also found no correlation between effective dispersal and other-life history traits which suggests no dispersal/life-history syndromes in the species investigated. One aspect that was not assessed was the impact of density dependence on pace-of-life and effective dispersal, largely as this was a first step in assessing relationship of dispersal with pace-of-life at different scales. However, the authors do acknowledge the importance of future studies incorporating density dependence and that such studies could potentially lead to more generalizable understanding of pace-of-life and dispersal within Trichogramma.

A pleasant addition was the link to potential implications for biocontrol. This addition showed an awareness by the authors of how insights into pace-of-life can have an applied component. The results of the study highlighted that selecting for specific lines of a species, to maximise a trait of interest at the cost of another, may not be as effective as selecting different species when implementing biocontrol. This is especially important as often single, established species used in biocontrol are favoured without consideration of the potential of other species which can lead to more efficient biocontrol.    

REFERENCES

Araya-Ajoy, Y.G., Bolstad, G.H., Brommer, J., Careau, V., Dingemanse, N.J. & Wright, J. (2018). Demographic measures of an individual's "pace of life": fecundity rate, lifespan, generation time, or a composite variable? Behavioral Ecology and Sociobiology, 72, 75.
https://doi.org/10.1007/s00265-018-2477-7
 
Bakewell, A.T., Davis, K.E., Freckleton, R.P., Isaac, N.J.B. & Mayhew, P.J. (2020). Comparing Life Histories across Taxonomic Groups in Multiple Dimensions: How Mammal-Like Are Insects? The American Naturalist, 195, 70-81.
https://doi.org/10.1086/706195
 
Guicharnaud, C., Groussier, G., Beranger, E., Lamy, L., Vercken, E. & Dahirel, M. (2023). Life-history traits, pace of life and dispersal among and within five species of Trichogramma wasps: a comparative analysis. bioRxiv, 2023.01.24.525360, ver. 3 peer-reviewed and recommended by Peer Community in Zoology.
https://doi.org/10.1101/2023.01.24.525360
 
Healy, K., Ezard, T.H.G., Jones, O.R., Salguero-Gómez, R. & Buckley, Y.M. (2019). Animal life history is shaped by the pace of life and the distribution of age-specific mortality and reproduction. Nature Ecology & Evolution, 3, 1217-1224.
https://doi.org/10.1038/s41559-019-0938-7
 
Salguero-Gómez, R., Jones, O.R., Jongejans, E., Blomberg, S.P., Hodgson, D.J., Mbeau-Ache, C., et al. (2016). Fast-slow continuum and reproductive strategies structure plant life-history variation worldwide. Proceedings of the National Academy of Sciences, 113, 230-235.
https://doi.org/10.1073/pnas.1506215112
 
Stearns, S.C. (1983). The Influence of Size and Phylogeny on Patterns of Covariation among Life-History Traits in the Mammals. Oikos, 41, 173-187.
https://doi.org/10.2307/3544261