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

In animals, male weapons such as antlers, horns, spurs, fangs, and tusks typically provide advantages in male contests and increase access to females, thereby enhancing reproductive success. However, such large and extravagant morphological structures are expected to come at a cost, potentially imposing trade-offs with life history traits, physiological functions, or certain behaviors (Emlen, 2001; Emlen, 2008). These costs should be manageable only by males in the best condition. The present study by Blackwell et al. (2024) examines this assumption through a comprehensive study on the European earwig, where males possess forceps-like cerci that vary widely in size within populations.

In the European earwig (Forficula auricularia), male forceps are used in male-male contests as weapons to deter competitors prior to mating (Styrsky & Rhein, 1999) or to interrupt mating pairs by non-copulating males (Forslund, 2000; Walker & Fell, 2001). Despite providing benefits in terms of mating success (Eberhard & Gutierrez, 1991; Tomkins & Brown, 2004), it remains unknown whether long or short forceps are associated with other important life-history traits.

In this laboratory study, Blackwell et al. (2024) investigated two European earwig populations, each divided into two subpopulations: one with the shortest forceps and one with the longest forceps. They examined the potential costs of long forceps on six different traits: one reproductive trait (sperm storage); three non-reproductive behavioral traits such as locomotor performance (involved in search for resources), fleeing reaction face to a risk (long forceps are supposed to be correlated with boldness), and aggregation behavior (European earwigs are facultative group-living organisms); and survival (when deprived of food and subsequently when exposed to an entomopathogenic fungus).

As males in the best condition are supposed to be those that can afford to develop large forceps, Blackwell et al. (2024) predicted that males with long forceps would perform better than those with short forceps across the investigated traits. However, their predictions were not validated, as no correlation between weapon size and male quality was detected in either population. Although the sample size is sometimes limited, the consistency of these results across different populations adds robustness to their conclusions.

By demonstrating that forceps length in the European earwig does not reliably indicate male quality, this paper challenges existing theories and highlights the complexity of evolutionary processes shaping morphological traits. Furthermore, the study raises important questions about the evolutionary mechanisms maintaining weapon size diversity, providing a fresh perspective that could stimulate further research and debate in the field, notably the search for other traits where costs might be incurred.

References

Blackwell, S.E.M., Pasquier, L., Dupont, S., Devers, S., Lécureuil, C. & Meunier, J. (2024). Relationship between weapon size and six key behavioural and physiological traits in males of the European earwig. bioRxiv, ver. 3 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2024.03.20.585871

Eberhard, W.G., & Gutierrez, E.E. (1991). Male dimorphisms in beetles and earwigs and the question of developmental constraints. Evolution, 45(1), 18–28. https://doi.org/10.2307/2409478

Emlen, D.J. (2001). Costs and the diversification of exaggerated animal structures. Science, 291(5508), 1534–1536. https://doi.org/10.1126/science.1056607

Emlen, D.J. (2008). The evolution of animal weapons. Annual Review of Ecology, Evolution, and Systematics, 39(1), 387–413. https://doi.org/10.1146/annurev.ecolsys.39.110707.173502

Forslund, P. (2000). Male-male competition and large size mating advantage in European earwigs, Forficula auricularia. Animal Behaviour, 59(4), 753–762. https://doi.org/10.1006/anbe.1999.1359

Styrsky, J.D., & Rhein, S.V. (1999). Forceps size does not determine fighting success in European earwigs. Journal of Insect Behavior, 12(4), 475–482. https://doi.org/10.1023/A:1020962606724

Tomkins, J.L., & Brown, G.S. (2004). Population density drives the local evolution of a threshold dimorphism. Nature, 431, 1099–1103. https://doi.org/10.1038/nature02936.1.

Walker, K.A., & Fell, R.D. (2001). Courtship roles of male and female European earwigs, Forficula auricularia L. (Dermaptera: Forficulidae), and sexual use of forceps. Journal of Insect Behavior, 14(1), 1–17. https://doi.org/10.1023/A:1007843227591

I recommend the Van Steenberge et al. study. With over 2000 endemic species, the East African cichlids are a well-established model system in speciation research (Salzburger 2018) and several models have been proposed and tested to explain how these radiations formed (Kocher 2004). Hybridization was shown to be a main driver of the rapid speciation and adaptive radiations of the East African Cichlid fishes (Seehausen 2004). However, it is obvious that unrestrained hybridization also has the potential to reduce taxonomic diversity by erasing species barriers. In the classical model of cichlid evolution, special emphasis was placed on mate preference (Kocher 2004). However, no attention was placed on species recognition, which was implicitly assumed. There is, however, more research needed on what species recognition means, especially in radiating lineages such as cichlids. In a previous study, Nevado et al. 2011 found traces of asymmetrical hybridization between members of the Lake Tanganyika radiation: the genus Ophthalmotilapia. This recommended study by Van Steenberge et al. is based on Nevado et al. (2011), which detected that in one genus of Ophthalmotilapia mitochondrial DNA ‘typical’ for one of the four species (O. nasuta) was also found in three other species (O. ventralis, O. heterodonta, and O. boops). The authors suggested that this could be explained by the fact that females of the three other species accepted O. nasuta males, but that O. nasuta females were more selective and accepted only conspecifc males. This could hence be due to asymmetric mate preferences, or by asymmetric abilities for species recognition. 

This is exactly what the current study by Van Steenberge et al. did. They tested the latter hypothesis by presenting females of two different Ophthalmotilapia species with con- and heterospecific males. This was tested through experiments, making use of wild specimens of two species: O. nasuta and O. ventralis. The authors assumed that if they performed classical “choice-experiments”, they would not notice the recognition effects, given that females would just select preferred, most likely conspecific, males. Instead, specimens were only briefly presented to other fishes since the authors wanted to compare differences in the ability for ‘species recognition’. In this, the authors followed Mendelson and Shaw (2012) who used “a measurable difference in behavioural response towards conspecifics as compared to heterospecifics’’ as a definition for recognition. Instead of the focus on selection/preference, they investigated if females of different species behaved differently, and hence detected the difference between conspecific and heterospecific males. This was tested by a short (15 minutes) exposure to another fish in an isolated part of the aquarium. Recognition was defined as the ‘difference in a particular behaviour between the two conditions’. What was monitored was the swimming behaviour and trajectory (1 image per second) together with known social behaviours of this genus. The selection of these behaviours was further facilitated based on experimental set-ups of reproductive behaviour or the same species previously described by the same research team (Kéver et al. 2018).

The result was that O. nasuta females, for which it was expected that they would not hybridize, showed a different behaviour towards a con- or a heterospecific male. They interacted less with males of the other species. What was unexpected is that there was no difference in behaviour of the females whether they recognized a male or (control) female of their own species. This suggests that they did not detect differences in reproductive behaviour, but rather in the interactions between conspecifics. For females of O. ventralis, for which there are indications for hybridization in the wild, they did not find a difference in behaviour. Females of this species behaved identically with respect to the right and wrong males as well as towards the control females. Interestingly is thus that a complex pattern between species in the wild could be (partially) explained by the behaviour/interaction at first impression of the individuals of these species. 

References

Kéver L, Parmentier E, Derycke S, Verheyen E, Snoeks J, Van Steenberge M, Poncin P (2018) Limited possibilities for prezygotic barriers in the reproductive behaviour of sympatric Ophthalmotilapia species (Teleostei, Cichlidae). Zoology, 126, 71–81. https://doi.org/10.1016/j.zool.2017.12.001

Kocher TD (2004) Adaptive evolution and explosive speciation: the cichlid fish model. Nature Reviews Genetics, 5, 288–298. https://doi.org/10.1038/nrg1316

Mendelson TC, Shaw KL (2012) The (mis)concept of species recognition. Trends in Ecology & Evolution, 27, 421–427. https://doi.org/10.1016/j.tree.2012.04.001

Nevado B, Fazalova V, Backeljau T, Hanssens M, Verheyen E (2011) Repeated Unidirectional Introgression of Nuclear and Mitochondrial DNA Between Four Congeneric Tanganyikan Cichlids. Molecular Biology and Evolution, 28, 2253–2267. https://doi.org/10.1093/molbev/msr043

Salzburger W (2018) Understanding explosive diversification through cichlid fish genomics. Nature Reviews Genetics, 19, 705–717. https://doi.org/10.1038/s41576-018-0043-9

Seehausen O (2004) Hybridization and adaptive radiation. Trends in Ecology & Evolution, 19, 198–207. https://doi.org/10.1016/j.tree.2004.01.003

Steenberge MV, Jublier N, Kéver L, Gresham S, Derycke S, Snoeks J, Parmentier E, Poncin P, Verheyen E (2022) The initial response of females towards congeneric males matches the propensity to hybridise in Ophthalmotilapia. bioRxiv, 2021.08.07.455508, ver. 3 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2021.08.07.455508

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

References

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

It is now widely accepted that anthropogenic climate change is a severe threat to biodiversity, ecosystem function and associated ecosystem services. Assessing the vulnerability of species and predicting their response to future changes has become a priority for environmental biology (Williams et al. 2020).

Over the last few decades, oxygen concentrations in both the open ocean and coastal waters have been declining steadily as the result of multiple anthropogenic activities. This global trends towards hypoxia is expected to continue in the future, causing a host of negative effects on marine ecosystems. Oxygen is indeed crucial to many biological processes in the ocean, and its decrease could have strong impacts on biogeochemical cycles, and therefore on marine productivity and biodiversity (Breitburg et al. 2018).

Whenever facing such drastic environmental changes, all organisms are expected to have some intrinsic ability to adapt. At shorter than evolutionary timescales, ecological plasticity and the eco-physiological processes that sustain it could constitute important adaptive mechanisms (Williams et al. 2020)

Marine sponges seem particularly well-adapted to oxygen deficiency, as some species can survive seasonal anoxia for several months. This paper by Strehlow et al. (2023) examines the mechanisms allowing this exceptional tolerance. Focusing on two species of sponges, they used transcriptomics to assess how gene expression by sponges, by their mitochondria, or by their unique and species-specific microbiome could facilitate this trait. Their results suggest that sponge holobionts maintain metabolic activity under anoxic conditions while displaying shock response, therefore not supporting the hypothesis of sponge dormancy. Furthermore, hypoxia and anoxia seemed to influence gene expression in different ways, highlighting the complexity of sponge response to deoxygenation. As often, their exciting results raise as many questions as they provide answers and pave the way for more research regarding how anoxia tolerance in marine sponges could give them an advantage in future oceanic environmental conditions.

References

Breitburg et al. (2018): Declining oxygen in the global ocean and coastal waters. Science 359, eaam7240. https://doi.org/10.1126/science.aam7240 

Strehlow et al. (2023): Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxia. bioRxiv, 2023.02.27.530229, ver. 4 peer-reviewed and recommended by Peer Community in Zoology.  https://doi.org/10.1101/2023.02.27.530229 

Williams et al. (2008) Towards an Integrated Framework for Assessing the Vulnerability of Species to Climate Change. PLOS Biology 6(12): e325. https://doi.org/10.1371/journal.pbio.0060325 

Williams et al. (2020):  Research priorities for natural ecosystems in a changing global climate. Global Change Biology 26: 410–416. https://doi.org/10.1111/gcb.14856