Whiteflies are serious global pests that feed on phloem sap of many agricultural crop plants. Like other phloem feeders, whiteflies rely on a primary-symbiont to supply their poor, sugar-based diet. Over time, the genomes of primary-symbionts become degraded, and they are either been replaced or complemented by co-hosted secondary-symbionts (McCutcheon and Moran 2012). In Bemisia tabaci species complex, the primary-symbiont is Candidatus Portiera aleyrodidarium, with seven secondary-symbionts that have been described to date. The prevalence and dynamics of these secondary-symbionts have been studied in various whitefly populations and genetic groups around the world, and certain combinations are determined under specific biotic and environmental factors (Zchori-Fein et al. 2014).

To understand the potential metabolic or other interactions of various secondary-symbionts with Ca. Portiera aleyrodidarium and the hosts, Mouton et al. used metabarcoding approach and diagnostic PCR confirmation, to describe symbiont compositions in a collection of whiteflies from eight populations with four genetic groups in Burkina Faso. They found that one of the previously recorded secondary-symbiont from Asian whitefly populations, Candidatus Hemipteriphilus asiaticus, is also found in the tested African whiteflies. The newly identified Ca. Hemipteriphilus asiaticus forms a different strain than the ones described in Asia, and is found in high prevalence in six of the tested populations and in three genetic groups. They also showed that Portiera densities are not affected by the presence of Ca. Hemipteriphilus asiaticus. The authors suggest that based on its high prevalence, Ca. Hemipteriphilus asiaticus may benefit certain whitefly populations, however, there is no attempt to test this assumption or to relate it to environmental factors, or to identify the source of introduction.

Mouton et al. bring new perspectives to the study of complex hemipteran symbioses, emphasizing the need to use both unbiased approaches such as metabarcoding, together with a priori methods such as PCR, in order to receive a complete description of symbiont population structures. Their findings are awaiting future screens for this secondary-symbiont, as well as its functional genomics and experimental manipulations to clarify its role. Discoveries on whitefly-symbionts delicate interactions are required to develop alternative control strategies for this worldly devastating pest.

References

McCutcheon JP, Moran NA (2012) Extreme genome reduction in symbiotic bacteria. Nature Reviews Microbiology, 10, 13–26. https://doi.org/10.1038/nrmicro2670

Mouton L, Henri H, Romba R, Belgaidi Z, Gnankiné O, Vavre F (2022) Analyses of symbiotic bacterial communities in the plant pest Bemisia tabaci reveal high prevalence of Candidatus Hemipteriphilus asiaticus on the African continent. bioRxiv, 2021.10.06.463217, ver. 3 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2021.10.06.463217

Zchori-Fein E, Lahav T, Freilich S (2014) Variations in the identity and complexity of endosymbiont combinations in whitefly hosts. Frontiers in Microbiology, 5. https://doi.org/10.3389/fmicb.2014.00310

Human African Trypanosomiasis (HAT), or sleeping sickness, is caused by trypanosome parasites. In sub-Saharan Africa, two forms are present, Trypanosoma brucei gambiense and T. b. rhodesiense, the former responsible for 95% of reported cases. The parasites are transmitted through a vector, Genus Glossina, also known as tsetse, which means fly in Tswana, a language from southern Africa. Through a blood meal, tsetse picks up the parasite from infected humans or animals (in animals, the parasite causes Animal African Trypanosomiasis or nagana disease). Through medical interventions and vector control programs, the burden of the disease has drastically reduced over the past two decades, so the WHO neglected tropical diseases road map targets the interruption of transmission (zero cases) for 2030 (WHO 2022).

Meaningful vector control programs utilize traps for the removal of animals and for surveillance, along with different methods of spraying insecticides. However, in existing HAT risk areas, it will be essential to understand the ecology of the vector species to implement control programs in a way that areas cleared from the vector will not be reinvaded from other populations. Thus, it will be crucial to understand basic population genetics parameters related to population structure and subdivision, migration frequency and distances, population sizes, and the potential for sex-biased dispersal. The authors utilize genotyping using nine highly polymorphic microsatellite markers of samples from Chad collected in differently affected regions and at different time points (Ravel et al., 2023). Two major HAT zones exist that are targeted by vector control programs, namely Madoul and Maro, while two other areas, Timbéri and Dokoutou, are free of trypanosomes. Samples were taken before vector control programs started.

The sex ratio was female-biased, most strongly in Mandoul and Maro, the zones with the lowest population density. This could be explained by resource limitation, which could be the hosts for a blood meal or the sites for larviposition. Limited resources mean that females must fly further, increasing the chance that more females are caught in traps. 

The effective population densities of Mandoul and Maro were low. However, there was a convergence of population density and trapping density, which might be explained by the higher preservation of flies in the high-density areas of Timbéri and Dokoutou after the first round of sampling, which can only be tested using a second sampling. 

The dispersal distances are the highest recorded so far, especially in Mandoul and Maro, with 20-30 km per generation. However, in Timbéri and Dokoutou, which are 50 km apart, very little exchange occurs (approx. 1-2 individuals every six months). A major contributor to this is the massive destruction of habitat that started in the early 1990s and left patchily distributed and fragmented habitats. The Mandoul zone might be safe from reinvasion after eradication, as for a successful re-establishment, either a pair of a female and male or a pregnant female are required. As the trypanosome prevalence amongst humans was 0.02 and of tsetse 0.06 (Ibrahim et al., 2021) before interventions began, medical interventions and vector control might have further reduced these levels, making a reinvasion and subsequent re-establishment of HAT very unlikely. Maro is close to the border of the Central African Republic, and the area has not been well investigated concerning refugee populations of tsetse, which could contribute to a reinvasion of the Maro zone. The higher level of genetic heterogeneity of the Maro population indicates that invasions from neighboring populations are already ongoing. This immigration could also be the reason for not detecting the bottleneck signature in the Maro population. 

The two HAT areas need different levels of attention while implementing vector eradication programs. While Madoul is relatively safe against reinvasion, Maro needs another type of attention, as frequent and persistent immigration might counteract eradication efforts. Thus, it is recommended that continuous tsetse suppression needs to be implemented in Maro.  

This study shows nicely that an in-depth knowledge of the processes within and between populations is needed to understand how these populations behave. This can be used to extrapolate, make predictions, and inform the organisations implementing vector control programs to include valuable adjustments, as in the case of Maro. Such integrative approaches can help prevent the failure of programs, potentially saving costs and preventing infections of humans and animals who might die if not treated.

References

Ibrahim MAM, Weber JS, Ngomtcho SCH, Signaboubo D, Berger P, Hassane HM, Kelm S (2021) Diversity of trypanosomes in humans and cattle in the HAT foci Mandoul and Maro, Southern Chad- Southern Chad-A matter of concern for zoonotic potential? PLoS Neglected Tropical Diseases, 15, e000 323. https://doi.org/10.1371/journal.pntd.0009323

Ravel S, Mahamat MH, Ségard A, Argiles-Herrero R, Bouyer J, Rayaisse JB, Solano P, Mollo BG, Pèka M, Darnas J, Belem AMG, Yoni W, Noûs C, de Meeûs T (2023) Population genetics of Glossina fuscipes fuscipes from southern Chad. Zenodo, ver. 9 peer-reviewed and recommended by PCI Zoology. https://doi.org/10.5281/zenodo.7763870

WHO (2022) Trypanosomiasis, human African (sleeping sickness). https://www.who.int/news-room/fact-sheets/detail/trypanosomiasis-human-african-(sleeping-sickness), retrieved 17. March 2023

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

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

Understanding how organisms are affected by environmental variations is a central question in ecophysiology and evolutionary ecology, particularly in the context of global changes(Fuller et al., 2016). Environmental variations challenge organisms' ability to maintain homeostasis leading to divergent adaptations between habitat specialists and generalists (Kawecki and Ebert, 2004). The article by (Keilani et al.) (2024) presents an original contribution to this field by focusing on the response to dry conditions in two rodent species from semi-arid regions of South Africa. The two species, Rhabdomys bechuanae and R.dilectus dilectus, have different environmental niches : R.dilectus dilectus occurring in mesic habitats while R. bechuanae is found in semi-arid and arid habitats. Previous studies highlighted morphological and behavioral adaptations to arid conditions in R. bechuanae (Dufour et al., 2019), the current study focuses on the physiological responses of the two species to seasonal dry conditions. By analyzing body condition, markers of kidney and liver functions, and habitat characteristics the authors aim to understand how aridity impacts parapatric populations of the two species. They hypothesize that i) the aridity of the habitat tend to increase during the dry season, ii) both species can adjust their physiology to dry conditions thanks to phenotypic plasticity, and iii)  R. bechuanae, having evolved in arid environments, will cope better with dry conditions than R. d. dilectus.
Consistent with their prediction, Keilani et al (2024) found physiological divergence between the two species. They also observed six blood markers (out of 12 tested) showing significant temporal changes, indicating resource depletion as the dry season progressed, even though the year of study was influenced by a relatively mild La Niña event (i.e. wet year). Both species displayed similar physiological responses to the dry conditions, such as reduced blood albumin level by the end of the dry season, confirming albumin as a reliable indicator of malnutrition and nutrient deficiency (AL Eissa et al., 2012). In terms of interspecific differences, R. bechuanae exhibited better water regulation, with lower sodium, potassium, and total bilirubin levels, which may indicate adaptation to drier environments. The study concludes that R. bechuanae appears better adapted to cope with arid conditions, highlighting the importance of physiological studies in understanding species' responses to climate change, and suggests that harsher dry seasons could further challenge R. d. dilectus, particularly in semi-arid zones. This study underscores the value of studying species in their natural environments to fully understand the scope and limitations of their responses to environmental changes.

References

Dufour, C.M.S., Pillay, N., Avenant, N., Watson, J., Loire, E., and Ganem, G. (2019) Habitat characteristics and species interference influence space use and nest-site occupancy: implications for social variation in two sister species. Oikos128: 503-516.
https://doi.org/10.1111/oik.05357 
 
AL Eissa, M.S., Saad, A., Al Farraj, S.A., Saud, A.A., Al Dahmash, B., and Hamad, A.Y. (2012) Seasonal variation effects on the composition of blood in Nubian ibex (Capra nubiana) in Saudi Arabia. Afr J Biotechnol 11: 1283-1286.
https://doi.org/10.5897/AJB11.2004
 
Fuller, A., Mitchell, D., Maloney, S.K., and Hetem, R.S. (2016) Towards a mechanistic understanding of the responses of large terrestrial mammals to heat and aridity associated with climate change. Climate Change Responses 3: 10.
https://doi.org/10.1186/s40665-016-0024-1 

Hamilcar S. Keilani, Nico L. Avenant, Pierre Caminade, Neville Pillay, Guila Ganem (2024) Negative impact of mild arid conditions on a rodent revealed using a physiological approach in natura. bioRxiv, ver.9 peer-reviewed and recommended by PCI Zoology
https://doi.org/10.1101/2024.03.11.583554