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14 Nov 2023
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Time-course of antipredator behavioral changes induced by the helminth Pomphorhynchus laevis in its intermediate host Gammarus pulex: the switch in manipulation according to parasite developmental stage differs between behaviors

Exploring manipulative strategies of a trophically-transmitted parasite across its ontogeny

Recommended by based on reviews by Adèle Mennerat and 1 anonymous reviewer

The intricate relationships between parasites and their hosts often involve a choreography of behavioral changes, with parasites manipulating their hosts in a way that enhances - or seemingly enhances – their transmission (Hughes et al., 2012; Moore, 2002; Poulin, 2010). Host manipulation is increasingly acknowledged as a pervasive adaptive transmission strategy employed by parasites, and as such is one of the most remarkable manifestations of the extended phenotype (Dawkins, 1982).

In this laboratory study, Rigaud et al. (2023) delved into the time course of antipredator behavioral modifications induced by the acanthocephalan Pomphorhynchus laevis in its amphipod intermediate host Gammarus pulex. This system has a good foundation of prior knowledge (Bakker et al., 2017; Fayard et al., 2020; Perrot-Minnot et al., 2023), nicely drawn upon for the present work. This parasite orchestrates a switch from predation suppression, during the noninfective phase, to predation enhancement upon maturation. Specifically, G. pulex infected with the non-infective acanthella stage of the parasite can exhibit increased refuge use and reduced activity compared to uninfected individuals (Dianne et al., 2011, 2014), leading to decreased predation by trout (Dianne et al., 2011). In contrast, upon reaching the infective cystacanth stage, the parasite can enhance the susceptibility of its host to trout predation (Dianne et al., 2011).

The present work aimed to understand the temporal sequence of these behavioral changes across the entire ontogeny of the parasite. The results confirmed the protective role of P. laevis during the acanthella stage, wherein infected amphipods exhibited heightened refuge use. This protective manipulation, however, became significant only later in the parasite's ontogeny, suggesting a delayed investment strategy, possibly influenced by the extended developmental time of P. laevis. The protective component wanes upon reaching the cystacanth stage, transitioning into an exposure strategy, aligning with theoretical predictions and previous empirical work (Dianne et al., 2011; Parker et al., 2009). The switch was behavior-specific. Unlike the protective behavior, a decline in the amphipod activity rate manifested early in the acanthella stage and persisted throughout development, suggesting potential benefits of reduced activity for the parasite across multiple stages. Furthermore, the findings challenge previous assumptions regarding the condition-dependency of manipulation, revealing that the parasite-induced behavioral changes predominantly occurred in the presence of cues signaling potential predators. Finally, while amphipods infected with acanthella stages displayed survival rates comparable to their uninfected counterparts, increased mortality was observed in those infected with cystacanth stages.

Understanding the temporal sequence of host behavioral changes is crucial for deciphering whether it is adaptive to the parasite or not. This study stands out for its meticulous examination of multiple behaviors over the entire ontogeny of the parasite highlighting the complexity and condition-dependent nature of manipulation. The protective-then-expose strategy emerges as a dynamic process, finely tuned to the developmental stages of the parasite and the ecological challenges faced by the host. The delayed emergence of protective behaviors suggests a strategic investment by the parasite, with implications for the host's survival and the parasite's transmission success. The differential impact of infection on refuge use and activity rate further emphasizes the need for a multidimensional approach in studying parasitic manipulation (Fayard et al., 2020). This complexity demands further exploration, particularly in deciphering how trophically-transmitted parasites shape the behavioral landscape of their intermediate hosts and its temporal dynamic (Herbison, 2017; Perrot-Minnot & Cézilly, 2013).  As we discover the many subtleties of these parasitic manipulations, new avenues of research are unfolding, promising a deeper understanding of the ecology and evolution of host-parasite interactions.


Bakker, T. C. M., Frommen, J. G., & Thünken, T. (2017). Adaptive parasitic manipulation as exemplified by acanthocephalans. Ethology, 123(11), 779–784.

Dawkins, R. (1982). The extended phenotype: The long reach of the gene (Reprinted). Oxford University Press.

Dianne, L., Perrot-Minnot, M.-J., Bauer, A., Gaillard, M., Léger, E., & Rigaud, T. (2011). Protection first then facilitation: A manipulative parasite modulates the vulnerability to predation of its intermediate host according to its own developmental stage. Evolution, 65(9), 2692–2698.

Dianne, L., Perrot-Minnot, M.-J., Bauer, A., Guvenatam, A., & Rigaud, T. (2014). Parasite-induced alteration of plastic response to predation threat: Increased refuge use but lower food intake in Gammarus pulex infected with the acanothocephalan Pomphorhynchus laevis. International Journal for Parasitology, 44(3–4), 211–216.

Fayard, M., Dechaume‐Moncharmont, F., Wattier, R., & Perrot‐Minnot, M. (2020). Magnitude and direction of parasite‐induced phenotypic alterations: A meta‐analysis in acanthocephalans. Biological Reviews, 95(5), 1233–1251.

Herbison, R. E. H. (2017). Lessons in Mind Control: Trends in Research on the Molecular Mechanisms behind Parasite-Host Behavioral Manipulation. Frontiers in Ecology and Evolution, 5, 102.

Hughes, D. P., Brodeur, J., & Thomas, F. (2012). Host manipulation by parasites. Oxford university press.

Moore, J. (2002). Parasites and the behavior of animals. Oxford University Press.

Parker, G. A., Ball, M. A., Chubb, J. C., Hammerschmidt, K., & Milinski, M. (2009). When should a trophically transmitted parasite manipulate its host? Evolution, 63(2), 448–458.

Perrot-Minnot, M.-J., & Cézilly, F. (2013). Investigating candidate neuromodulatory systems underlying parasitic manipulation: Concepts, limitations and prospects. Journal of Experimental Biology, 216(1), 134–141.

Perrot-Minnot, M.-J., Cozzarolo, C.-S., Amin, O., Barčák, D., Bauer, A., Filipović Marijić, V., García-Varela, M., Servando Hernández-Orts, J., Yen Le, T. T., Nachev, M., Orosová, M., Rigaud, T., Šariri, S., Wattier, R., Reyda, F., & Sures, B. (2023). Hooking the scientific community on thorny-headed worms: Interesting and exciting facts, knowledge gaps and perspectives for research directions on Acanthocephala. Parasite, 30, 23.

Poulin, R. (2010). Parasite Manipulation of Host Behavior. In Advances in the Study of Behavior (Vol. 41, pp. 151–186). Elsevier.

Rigaud, T., Balourdet, A., & Bauer, A. (2023). Time-course of antipredator behavioral changes induced by the helminth Pomphorhynchus laevis in its intermediate host Gammarus pulex: The switch in manipulation according to parasite developmental stage differs between behaviors. bioRxiv, ver. 6 peer-reviewed and recommended by Peer Community in Zoology.

Time-course of antipredator behavioral changes induced by the helminth *Pomphorhynchus laevis* in its intermediate host *Gammarus pulex*: the switch in manipulation according to parasite developmental stage differs between behaviorsThierry Rigaud, Aude Balourdet, Alexandre Bauer<p style="text-align: justify;">Many trophically transmitted parasites with complex life cycles manipulate their intermediate host antipredatory defenses in ways facilitating their transmission to final host by predation. Some parasites also prote...Aquatic, Behavior, Crustacea, Invertebrates, ParasitologyThierry Lefevre2023-06-20 15:49:32 View
21 Jun 2023
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Life-history traits, pace of life and dispersal among and within five species of Trichogramma wasps: a comparative analysis

The relationship between dispersal and pace-of-life at different scales

Recommended by based on reviews by Mélanie Thierry and 1 anonymous reviewer

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.    


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.
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.
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.
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.
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.
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.

Life-history traits, pace of life and dispersal among and within five species of *Trichogramma* wasps: a comparative analysisChloé Guicharnaud, Géraldine Groussier, Erwan Beranger, Laurent Lamy, Elodie Vercken, Maxime Dahirel<p>Major traits defining the life history of organisms are often not independent from each other, with most of their variation aligning along key axes such as the pace-of-life axis. We can define a pace-of-life axis structuring reproduction and de...Biology, Ecology, Insecta, Invertebrates, Life historiesJacques Deere2023-01-25 18:15:20 View
27 Apr 2023
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Climate of origin influences how a herbivorous mite responds to drought-stressed host plants

Not all spider-mites respond in the same way to drought

Recommended by and based on reviews by Bastien Castagneyrol and 2 anonymous reviewers

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.

du Plessis, A. (2019). Current and Future Water Scarcity and Stress. In: Water as an Inescapable Risk. Springer Water. Springer, Cham.
Gibert, J.P. Temperature directly and indirectly influences food web structure. Sci Rep 9, 5312 (2019).
Liu, O. R., & Gaines, S. D. (2022). Environmental context dependency in species interactions. Proceedings of the National Academy of Sciences, 119(36), e2118539119.
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.
O'Connor, M.I. (2009), Warming strengthens an herbivore-plant interaction. Ecology, 90: 388-398.
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.

Climate of origin influences how a herbivorous mite responds to drought-stressed host plantsAlain Migeon, Philippe Auger, Odile Fossati-Gaschignard, Ruth A. Hufbauer, Maëva Miranda, Ghais Zriki, Maria Navajas<p style="text-align: justify;">Drought associated with climate change can stress plants, altering their interactions with phytophagous arthropods. Drought not only impacts cultivated plants but also their parasites, which in some cases are favore...Acari, Ecology, Life historiesInês Fragata2021-10-22 14:56:03 View
27 Apr 2023
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Brood thermoregulation effectivenessis positively linked to the amount of brood but not to the number of bees in honeybee colonies

Precision and accuracy of honeybee thermoregulation

Recommended by based on reviews by Jakob Wegener and Christopher Mayack

The Western honeybee, Apis mellifera L., is one of the best-studied social insects. It shows a reproductive division of labour, cooperative brood care, and age-related polyethism. Furthermore, honeybees regulate the temperature in the hive. Although bees are invertebrates that are usually ectothermic, this is still true for individual worker bees, but the colony maintains a very narrow range of temperature, especially within the brood nest. This is quite important as the development of individuals is dependent on ambient temperature, with higher temperatures resulting in accelerated development and vice versa. In honeybees, a feedback mechanism couples developmental temperature and the foraging behaviour of the colony and the future population development (Tautz et al., 2003). Bees raised under lower temperatures are more likely to perform in-hive tasks, while bees raised under higher temperatures are better foragers. To maintain optimal levels of worker population growth and foraging rates, it is adaptive to regulate temperature to ensure optimal levels of developing brood. Moreover, this allows honeybees to decouple the internal developmental processes from ambient temperatures enhancing the ecological success of the species. 

In every system of thermoregulation, whether it is endothermic under the utilization of energetic resources as in mammals or the honeybee or ectothermic as in lower vertebrates and invertebrates through differential exposure to varying environmental temperature gradients, there is a need for precision (low variability) and accuracy (hitting the target temperature). However, in honeybees, the temperature is regulated by workers through muscle contraction and fanning of the wings and thus, a higher number of workers could be better at achieving precise and accurate temperature within the brood nest. Alternatively, the amount of brood could trigger responses with more brood available, a need for more precise and accurate temperature control. The authors aimed at testing these two important factors on the precision and accuracy of within-colony temperature regulation by monitoring 28 colonies equipped with temperature sensors for two years (Godeau et al., 2023).

They found that the number of brood cells predicted the mean temperature (accuracy of thermoregulation). Other environmental factors had a small effect. However, the model incorporating these factors was weak in predicting the temperature as it overestimated temperatures in lower ranges and underestimated temperatures in higher ranges. In contrast, the variability of the target temperature (precision of thermoregulation) was positively affected by the external temperature, while all other factors did not show a significant effect. Again, the model was weak in predicting the data. Overall colony size measured in categories of the number of workers and the number of brood cells did not show major differences in variability of the mean temperature, but a slight positive effect for the number of bees on the mean temperature. 

Unfortunately, the temperature was a poor predictor of colony size. The latter is important as the remote control of beehives using Internet of Things (IoT) technologies get more and more incorporated into beekeeping management. These IoT technologies and their success are dependent on good proxies for the control of the status of the colony. Amongst the factors to monitor, the colony size (number of bees and/or amount of brood) is extremely important, but temperature measurements alone will not allow us to predict colony sizes. Nevertheless, this study showed clearly that the number of brood cells is a crucial factor for the accuracy of thermoregulation in the beehive, while ambient temperature affects the precision of thermoregulation. In the view of climate change, the latter factor seems to be important, as more extreme environmental conditions in the future call for measures of mitigation to ensure the proper functioning of the bee colony, including the maintenance of homeostatic conditions inside of the nest to ensure the delivery of the ecosystem service of pollination.


Godeau U, Pioz M, Martin O, Rüger C, Crauser D, Le Conte Y, Henry M, Alaux C (2023) Brood thermoregulation effectiveness is positively linked to the amount of brood but not to the number of bees in honeybee colonies. EcoEvoRxiv, ver. 5 peer-reviewed and recommended by Peer Community in Zoology. 

Tautz J, Maier S, Claudia Groh C, Wolfgang Rössler W, Brockmann A (2003) Behavioral performance in adult honey bees is influenced by the temperature experienced during their pupal development. PNAS 100: 7343–7347.

Brood thermoregulation effectivenessis positively linked to the amount of brood but not to the number of bees in honeybee coloniesUgoline Godeau, Maryline Pioz, Olivier Martin, Charlotte Rüger, Didier Crauser, Yves Le Conte, Mickael Henry, Cédric Alaux<p style="text-align: justify;">To ensure the optimal development of brood, a honeybee colony needs to regulate its temperature within a certain range of values (thermoregulation), regardless of environmental changes in biotic and abiotic factors....Biology, Conservation biology, Demography/population dynamics, Ecology, InsectaMichael Lattorff Mauricio Daniel Beranek2022-07-06 09:20:10 View
26 Apr 2023
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Microbiome mediated tolerance to biotic stressors: a case study of the interaction between a toxic cyanobacterium and an oomycete-like infection in Daphnia magna

Multi-stress responses depend on the microbiome in the planktonic crustacean Daphnia

Recommended by and based on reviews by Natacha Kremer and 2 anonymous reviewers

The critical role that gut microbiota play in many aspects of an animal’s life, including pathogen resistance, detoxification, digestion, and nutritional physiology, is becoming more and more apparent (Engel and Moran 2013; Lindsay et al., 2020). Gut microbiota recruitment and maintenance can be largely affected by the surrounding environment (Chandler et al., 2011; Callens et al., 2020). The environment may thus dictate gut microbiota composition and diversity, which in turn can affect organismal responses to stress. Only few studies have, however, taken the gut microbiota into account to estimate life histories in response to multiple stressors in aquatic systems (Macke et al., 2016). 

Houwenhuyse et al., investigate how the microbiome affects life histories in response to ecologically relevant single and multiple biotic stressors (an oomycete-like parasite, and a toxic cyanobacterium) in Daphnia magna (Houwenhuyse et al., 2023). Daphnia is an excellent model, because this aquatic system lends itself extremely well for gut microbiota transplantation and manipulation. This is due to the possibility to sterilize eggs (making them free of bacteria), horizontal transmission of bacteria from the environment, and the relative ease of culturing genetically similar Daphnia clones in large numbers. 

The authors use an elegant experimental design to show that the Daphnia gut microbial community differs when derived from a laboratory versus natural inoculum, the latter being more diverse. The authors subsequently show that key life history traits (survival, fecundity, and body size) depend on the stressors (and combination thereof), the microbiota (structure and diversity), and Daphnia genotype. A key finding is that Daphnia exposed to both biotic stressors show an antagonistic interaction effect on survival (being higher), but only in individuals containing laboratory gut microbiota. The exact mechanism remains to be determined, but the authors propose several interesting hypotheses as to why Daphnia with more diverse gut microbiota do less well. This could be due, for example, to increased inter-microbe competition or an increased chance of contracting opportunistic, parasitic bacteria. For Daphnia with less diverse laboratory gut microbiota, a monopolizing species may be particularly beneficial for stress tolerance. Alongside these interesting findings, the paper also provides extensive information about the gut microbiota composition (available in the supplementary files), which is a very useful resource for other researchers. 

Overall, this study reveals that multiple, interacting factors affect the performance of Daphnia under stressful conditions. Of importance is that laboratory studies may be based on simpler microbiota systems, meaning that stress responses measured in the laboratory may not accurately reflect what is happening in nature. 


Callens M, De Meester L, Muylaert K, Mukherjee S, Decaestecker E. The bacterioplankton community composition and a host genotype dependent occurrence of taxa shape the Daphnia magna gut bacterial community. FEMS Microbiology Ecology. 2020;96(8):fiaa128.

Chandler JA, Lang JM, Bhatnagar S, Eisen JA, Kopp A. Bacterial communities of diverse Drosophila species: ecological context of a host-microbe model system. PLOS Genetics. 2011;7(9):e1002272.

Engel P, Moran NA. The gut microbiota of insects - diversity in structure and function. FEMS Microbiology Reviews. 2013;37(5):699-735.

Houwenhuyse S, Bulteel L, Vanoverberghe I, Krzynowek A, Goel N et al. Microbiome mediated tolerance to biotic stressors: a case study of the interaction between a toxic cyanobacterium and an oomycete-like infection in Daphnia magna. 2023. OSF, ver. 2 peer-reviewed and recommended by Peer Community in Zoology.

Lindsay EC, Metcalfe NB, Llewellyn MS. The potential role of the gut microbiota in shaping host energetics and metabolic rate. Journal of Animal Ecology. 2020;89(11):2415-2426.

Macke E, Tasiemski A, Massol F, Callens M, Decaestecker E. Life history and eco-evolutionary dynamics in light of the gut microbiota. Oikos. 2017;126(4):508-531.

Microbiome mediated tolerance to biotic stressors: a case study of the interaction between a toxic cyanobacterium and an oomycete-like infection in *Daphnia magna*Shira Houwenhuyse*, Lore Bulteel*, Isabel Vanoverberghe, Anna Krzynowek, Naina Goel, Manon Coone, Silke Van den Wyngaert, Arne Sinnesael, Robby Stoks & Ellen Decaestecker<p style="text-align: justify;">Organisms are increasingly facing multiple, potentially interacting stressors in natural populations. The ability of populations coping with combined stressors depends on their tolerance to individual stressors and ...Aquatic, Biology, Crustacea, Ecology, Life histories, SymbiosisBertanne Visser2021-05-17 16:18:18 View
21 Mar 2023
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Population genetics of Glossina fuscipes fuscipes from southern Chad

Population genetics of tsetse, the vector of African Trypanosomiasis, helps informing strategies for control programs

Recommended by based on reviews by 2 anonymous reviewers

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.


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.

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.

WHO (2022) Trypanosomiasis, human African (sleeping sickness)., retrieved 17. March 2023

Population genetics of Glossina fuscipes fuscipes from southern ChadSophie Ravel, Mahamat Hissène Mahamat, Adeline Ségard, Rafael Argiles-Herrero, Jérémy Bouyer, Jean-Baptiste Rayaisse, Philippe Solano, Brahim Guihini Mollo, Mallaye Pèka, Justin Darnas, Adrien Marie Gaston Belem, Wilfrid Yoni, Camille Noûs, Thierr...<p>In Subsaharan Africa, tsetse flies (genus Glossina) are vectors of trypanosomes causing Human African Trypanosomiasis (HAT) and Animal African Trypanosomosis (AAT). Some foci of HAT persist in Southern Chad, where a program of tsetse control wa...Biology, Ecology, Evolution, Genetics/Genomics, Insecta, Medical entomology, Parasitology, Pest management, Veterinary entomologyMichael Lattorff Audrey Bras2022-04-22 11:25:24 View
09 Feb 2023
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A novel nematode species from the Siberian permafrost shares adaptive mechanisms for cryptobiotic survival with C. elegans dauer larva

A novel nematode species from the Siberian permafrost shares adaptive mechanisms for cryptobiotic survival with C. elegans dauer larva

Recommended by based on reviews by 3 anonymous reviewers

This article [1] investigated two nematode genera, Panagrolaimus and Plectus, from the Siberian permafrost to unravel the adaptations allowing them to survive cryptobiosis; radio carbon dating showed that the individuals of Panagrolaimus had been in cryobiosis in Siberia for as long as 46,000 years! 

I was impressed by the multidisciplinary approach of this study, including morphological as well as phylogenetic and -genomic analyses to describe a new species. In triploids as some of the species studied here, it is quite challenging to assemble a novel genome. The authors furthermore not only managed to successfully reanimate the Siberian specimens but could also expose them to repeated freezing and desiccation in the lab, not an easy task.

This study reports some amazing discoveries - comparing the molecular toolkits between C. elegans and Panagrolaimus and Plectus revealed that several components were orthologues. Likewise, some of the biochemical mechanisms for surviving freezing in the lab turned out to be similar for C. elegans and the Siberian nematodes. This study thus provides strong evidence that nematodes developed specific mechanisms allowing them to stay in cryobiosis over very long times.

A surprising additional experimental result concerns the well-studied C. elegans - dauer larvae of this species can stay viable much longer after periods of animated suspension than previously thought.

I highly recommend this article as it is an important contribution to the fields of evolution and molecular biology. This study greatly advanced our understanding of how nematodes could have adapted to cryobiosis. The applied techniques could also be useful for studying similar research questions in other organisms.


[1] Shatilovich A, Gade VR, Pippel M, Hoffmeyer TT, Tchesunov AV, Stevens L, Winkler S, Hughes GM, Traikov S, Hiller M, Rivkina E, Schiffer PH, Myers EW, Kurzchalia TV (2023) A novel nematode species from the Siberian permafrost shares adaptive mechanisms for cryptobiotic survival with C. elegans dauer larva. bioRxiv, 2022.01.28.478251, ver. 6 peer-reviewed and recommended by Peer Community in Zoology.

A novel nematode species from the Siberian permafrost shares adaptive mechanisms for cryptobiotic survival with C. elegans dauer larvaAnastasia Shatilovich, Vamshidhar R. Gade, Martin Pippel, Tarja T. Hoffmeyer, Alexei V. Tchesunov, Lewis Stevens, Sylke Winkler, Graham M. Hughes, Sofia Traikov, Michael Hiller, Elizaveta Rivkina, Philipp H. Schiffer, Eugene W Myers, Teymuras V. K...<p style="text-align: justify;">Some organisms in nature have developed the ability to enter a state of suspended metabolism called cryptobiosis1 when environmental conditions are unfavorable. This state-transition requires the execution of comple...Ecology, Evolution, Genetics/GenomicsIsa Schon2022-05-20 14:32:02 View
20 Dec 2022
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Non-target effects of ten essential oils on the egg parasitoid Trichogramma evanescens

Side effects of essential oils on pest natural enemies

Recommended by based on reviews by Olivier Roux and 2 anonymous reviewers

Integrated pest management relies on the combined use of different practices in time and/or space. The main objectives are to better control pests, not to induce too much selective pressure on resistance mechanisms present in pest populations and to minimize non-targeted effects on the ecosystem [1]. The efficiency of such a strategy requires at least additional or synergistic effects of chosen tools against targeted pest population in a specific environment. Any antagonistic effect on targeted or non-targeted organisms might reduce control effort to nil even worst.

Van Oudenhove et al [2] raised the question of the interaction between botanical pesticides (BPs) and egg parasitoids. Each of these two strategies used for pest management present advantages and are described as eco-friendly. First, the use of parasitoids is a great example of biological control and is massively used in a broad range of crop production in different ecological settings. Second, BPs, especially essential oils (EOs) used for a wide range of activities on pests (repellent, antifeedant, antiovipositant, ovicidal, larvicidal and simply pesticidal) present low-toxicity to non-target vertebrates and do not last too long in the environment. Combining these two strategies might be considered as a great opportunity to better pest control with minimized impact on environment. However, EOs used to target a wide range of pest might directly or indirectly affect parasitoids.

Van Oudenhove et al [2] focused their study on non-target effects of 10 essentials oils with pesticide potential on larval development and egg-seeking behaviour of five strains of the biocontrol agent Trichogramma evanescens. Within two laboratory experiments mimicing EOs fumigation (i.e. contactless EOs exposure), the authors evaluated (1) the toxicity of EOs on parasitoid development and (2) the repellent effect of these EOs on adult wasps. They confirmed that contactless exposure of EOs can (1) induce mortality during pre-imaginal development (more acute at the pupal stage) and (2) induce behavioural avoidance of EOs odour plume. These experiments ran onto five strains of T. evanescens also highlighted the variation of the effects of EOs among parasitoid strains.

The complex and dynamic interaction between pest, plant, parasitoid (a natural enemy) and their environment is disturbed by EOs. EOs plumes are also dynamic and variable upon the environmental conditions. The results of van Oudenhove et al. experimentally illustrate such a complexity by describing opposite effects (repellent and attractive) of the same EO on the behaviour of two T. evanescens strains. These contrasting results led us to question more broadly the non-target effects of pest management programs based on EOs fumigation on natural enemies.

Finally, the limits of this experimental study as discussed in the paper draw research avenues taking into account biotic variables such as plant chemical cues, odour plume dynamics, individual behavioural experiences and abiotic variables such as temperature, light and gravity [3] in laboratory, semi-field and field experiments. Facing such a complexity, modelling studies at fine scale in time and space have the operational objective to help farmers to choose the best IPM strategy regarding their environment (as illustrated for aphid population management in the recent review by Stell et al. [4]). But before such research effort to be undertaken, Van Oudenhove et al study [2] sounds like an alert for a cautious use of EOs in pest control programs that integrate biological control with parasitoids.



[1] Fauvergue, X. Biocontrôle Elements Pour Une Protection Agroecologique des Cultures; Éditions Quae: Versailles, France, 2020.

[2] van Oudenhove L, Cazier A, Fillaud M, Lavoir AV, Fatnassi H, Pérez G, Calcagno V. Non-target effects of ten essential oils on the egg parasitoid Trichogramma evanescens. bioRxiv 2022.01.14.476310, ver. 4 peer-reviewed and recommended by PCI Zoology.

[3] Victor Burte, Guy Perez, Faten Ayed, Géraldine Groussier, Ludovic Mailleret, Louise van Oudenhove and Vincent Calcagno (2022) Up and to the light: intra- and interspecific variability of photo- and geo-tactic oviposition preferences in genus Trichogramma, Peer Community Journal, 2: e3.

[4] Stell E, Meiss H, Lasserre-Joulin F, Therond O. Towards Predictions of Interaction Dynamics between Cereal Aphids and Their Natural Enemies: A Review. Insects 2022, 13, 479.

Non-target effects of ten essential oils on the egg parasitoid Trichogramma evanescensLouise van Oudenhove, Aurélie Cazier, Marine Fillaud, Anne-Violette Lavoir, Hicham Fatnassi, Guy Pérez, Vincent Calcagno<p style="text-align: justify;">Essential oils (EOs) are increasingly used as biopesticides due to their insecticidal potential. This study addresses their non-target effects on a biological control agent: the egg parasitoid <em>Trichogramma evane...Behavior, Biochemistry, Biocontrol, Biodiversity, Computer modelling, Conservation biology, Demography/population dynamics, Development, Ecology, Insecta, Insectivores, Invertebrates, Life histories, Methodology, Pest management, Theoretical biolo...Cedric Pennetier2022-01-31 16:05:32 View
30 Nov 2022
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A pipeline for assessing the quality of images and metadata from crowd-sourced databases.

Harnessing the full potential of iNaturalist and other databases

Recommended by based on reviews by Clive Hambler and Catherine Scott

The popularity of iNaturalist and other online biodiversity databases to which the general public and specialists alike contribute observations has skyrocketed in recent years (Dance 2022). The AI-based algorithms (computer vision) which provide the first identification of a given organism on an uploaded photograph have become very sophisticated, suggesting initial identifications often down to species level with a surprisingly high degree of accuracy. The initial identifications are then confirmed or improved by feedback from the community, which works particularly well for organismal groups to which many active community members contribute, such as the birds. Hence, providing initial observations and identifying observations of others, as well as browsing the recorded biodiversity for given locales or the range of occurrences of individual taxa has become a meaningful and satisfying experience for the interested naturalist. Furthermore, several research studies have now been published relying on observations uploaded to iNaturalist (Szentivanyi and Vincze 2022). However, using the enormous amount of natural history data available on iNaturalist in a systematic way has remained challenging, since this requires not only retrieving numerous observations from the database (in the hundreds or even thousands), but also some level of transparent quality control.

Billotte (2022) provides a protocol and R scripts for the quality assessment of downloaded observations from iNaturalist, allowing an efficient and reproducible stepwise approach to prepare a high-quality data set for further analysis. First, observations with their associated metadata are downloaded from iNaturalist, along with the corresponding entries from the Global Biodiversity Information Facility (GBIF). In addition, a taxonomic reference list is obtained (these are available online for many taxa), which is used to assess the taxonomic consistency in the dataset. Second, the geo-tagging is assessed by comparing the iNaturalist and GBIF metadata. Lastly, the image quality is assessed using pyBRISQUE. The approach is illustrated using spiders (Araneae) as an example. Spiders are a very diverse taxon and an excellent taxonomic reference list is available (World Spider Catalogue 2022). However, spiders are not well known to most non-specialists, and it is not easy to take good pictures of spiders without using professional equipment. Therefore, the ability of iNaturalist’s computer vision to provide identifications is limited to this date and the community of specialists active on iNaturalist is comparatively small. Hence, spiders are a good taxon to demonstrate how the pipeline results in a quality-controlled dataset based on crowed-sourced data. Importantly, the software employed is free to use, although inevitably, the initial learning curve to use R scripts can be steep, depending on prior expertise with R/RStudio. Furthermore, the approach is employable with databases other than iNaturalist.

In summary, Billotte's (2022) pipeline allows researchers to use the wealth of observations on iNaturalist and other databases to produce large metadata and image datasets of high-quality in a reproducible way. This should pave the way for more studies, which could include, for example, the assessment of range expansions of invasive species or the evaluation of the presence of endangered species, potentially supporting conservation efforts.


Billotte J (2022) A pipeline for assessing the quality of images and metadata from crowd-sourced databases. BiorXiv, 2022.04.29.490112, ver 5 peer reviewed and recommended by Peer Community In Zoology.

Dance A (2022) Community science draws on the power of the crowd. Nature, 609, 641–643.

Szentivanyi T, Vincze O (2022) Tracking wildlife diseases using community science: an example through toad myiasis. European Journal of Wildlife Research, 68, 74.

World Spider Catalog (2022). World Spider Catalog. Version 23.5. Natural History Museum Bern, online at

A pipeline for assessing the quality of images and metadata from crowd-sourced databases.Jackie Billotte<p style="text-align: justify;">Crowd-sourced biodiversity databases provide easy access to data and images for ecological education and research. One concern with using publicly sourced databases; however, is the quality of their images, taxonomi...Arachnids, Biodiversity, Biology, Conservation biology, Ecology, Insecta, InvertebratesMatthias Foellmer2022-05-03 00:18:23 View
28 Aug 2022
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A simple procedure to detect, test for the presence of stuttering, and cure stuttered data with spreadsheet programs

Improved population genetics parameters through control for microsatellite stuttering

Recommended by based on reviews by Thibaut Malausa, Fabien Halkett and Thierry Rigaud

Molecular markers have drastically changed and improved our understanding of biological processes. In combination with PCR, markers revolutionized the study of all organisms, even tiny insects, and eukaryotic pathogens amongst others. Microsatellite markers were the most prominent and successful ones. Their success started in the early 1990s. They were used for population genetic studies, mapping of genes and genomes, and paternity testing and inference of relatedness. Their popularity is based on some of their characteristics as codominance, the high polymorphism information content, and their ease of isolation (Schlötterer 2004). Still, microsatellites are the marker of choice for a range of non-model organisms as next-generation sequencing technologies produce a huge amount of single nucleotide polymorphisms (SNPs), but often at expense of sample size and higher costs.
The high level of polymorphism of microsatellite markers, which consist of one to six base-pair nucleotide motifs replicated up to 10 or 20 times, results from slippage events during DNA replication. Short hairpin loops might shorten the template strand or extend the new strand. However, such slippage events might occur during PCR amplification resulting in additional bands or peaks. Such stutter alleles often appear to differ by one repeat unit and might be hard to interpret but definitively reduce automated scoring of microsatellite results.
A standalone software package available to handle stuttering is Microchecker (van Oosterhout et al., 2004, which nowadays faces incompatibilities with updated versions of different operating systems. Thus, de Meeûs and Noûs (2022), in their manuscript, tackled the stuttering issue by developing an OS-independent analysis pipeline based on standard spreadsheet software such as Microsoft Office (Excel) or Apache Open Office (Calc). The authors use simulated populations differing in the mating system (pangamic, selfing (30%), clonal) and a different number of subpopulations and individuals per subpopulation to test for differences among the null model (no stuttering), a test population with 2 out of 20 loci (10%) with stuttering, and the latter with stuttering cured. Further to this, the authors also re-analyse data from previous studies utilising organisms differing in the mating system to understand whether control of stuttering changes major parameter estimates and conclusions of those studies.
Stuttering of microsatellite loci might result in increased heterozygote deficits. The authors utilise the FIS (inbreeding coefficient) as a tool to compare the different treatments of the simulated populations. Their method detected stuttering in pangamic and selfing populations, while the detection of stuttering in clonal organisms is more difficult. The cure for stuttering resulted in FIS values similar to those populations lacking stuttering. The re-analysis of four previously published studies indicated that the new method presented here is more accurate than Microchecker (van Oosterhout et al., 2004) in a direct comparison. For the Lyme disease-transmitting tick Ixodes scapularis (De Meeûs et al., 2021), three loci showed stuttering and curing these resulted in data that are in good agreement with pangamic reproduction. In the tsetse fly Glossina palpalis palpalis (Berté et al., 2019), two out of seven loci were detected as stuttering. Curing them resulted in decreased FIS for one locus, while the other showed an increased FIS, an indication of other problems such as the occurrence of null alleles. Overall, in dioecious pangamic populations, the method works well, and the cure of stuttering improves population genetic parameter estimates, although FST and FIS might be slightly overestimated. In monoecious selfers, the detection and cure work well, if other factors such as null alleles do not interfere. In clonal organisms, only loci with extremely high FIS might need a cure to improve parameter estimates.
This spreadsheet-based method helps to automate microsatellite analysis at very low costs and thus improves the accuracy of parameter estimates. This might certainly be very useful for a range of non-model organisms, parasites, and their vectors, for which microsatellites are still the marker of choice. 

Berté D, De Meeus T, Kaba D, Séré M, Djohan V, Courtin F, N'Djetchi KM, Koffi M, Jamonneau V, Ta BTD, Solano P, N’Goran EK, Ravel S (2019) Population genetics of Glossina palpalis palpalis in sleeping sickness foci of Côte d'Ivoire before and after vector control. Infection Genetics and Evolution 75, 103963.

de Meeûs T, Chan CT, Ludwig JM, Tsao JI, Patel J, Bhagatwala J, Beati L (2021) Deceptive combined effects of short allele dominance and stuttering: an example with Ixodes scapularis, the main vector of Lyme disease in the U.S.A. Peer Community Journal 1, e40.

de Meeûs T, Noûs C (2022) A simple procedure to detect, test for the presence of stuttering, and cure stuttered data with spreadsheet programs. Zenodo, v5, peer-reviewed and recommended by PCI Zoology.

Schlötterer C (2004) The evolution of molecular markers - just a matter of fashion? Nature Reviews Genetics 5, 63-69.

van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535-538.

A simple procedure to detect, test for the presence of stuttering, and cure stuttered data with spreadsheet programsThierry de Meeûs and Camille Noûs<p>Microsatellite are powerful markers for empirical population genetics, but may be affected by amplification problems like stuttering that produces heterozygote deficits between alleles with one repeat difference. In this paper, we present a sim...Acari, Ecology, Evolution, Genetics/Genomics, Helminthology, Invertebrates, Medical entomology, Molecular biology, Parasitology, Theoretical biology, Veterinary entomologyMichael Lattorff2021-12-06 14:30:47 View