Polar and subpolar regions are fragile environments, where the introduction of alien species may completely change ecosystem dynamics if the alien species become keystone species (e.g. Croll, 2005). The increasing number of human visits, together with climate change, are favouring the introduction and settling of new invaders to these regions, particularly in Antarctica (Hughes et al. 2015). Within this context, the joint use of Species Distribution Models (SDM) –to assess the areas potentially suitable for the aliens– with other measures of the potential to become successful invaders can inform on the need for devoting specific efforts to eradicate these new species before they become naturalized (e.g. Pertierra et al. 2016).
Bazzichetto et al. (2020) use data from a detailed inventory, SDMs and trait data altogether to assess the drivers of invasion success of six alien plants on Possession Island, in the remote sub-Antarctic archipelago of Crozet. SDMs have inherent limitations to describe different aspects of species distributions, including the fundamental niche and, with it, the areas that could host viable populations (Hortal et al. 2012). Therefore, their utility to predict future biological invasions is limited (Jiménez-Valverde et al. 2011). However, they can be powerful tools to describe species range dynamics if they are thoughtfully used by adopting conscious decisions about the techniques and data used, and interpreting carefully the actual implications of their results.
This is what Bazzichetto et al. (2020) do, using General Linear Models (GLM) –a technique well rooted in the original niche-based SDM theory (e.g. Austin 1990)– that can provide a meaningful description of the realized niche within the limits of an adequately sampled region. Further, as alien species share and are similarly affected by several steps of the invasion process (Richardson et al. 2000), these authors model the realized distribution of the six species altogether. This can be done through the recently developed joint-SDM, a group of techniques where the co-occurrence of the modelled species is explicitly taken into account during modelling (e.g. Pollock et al. 2014). Here, the addition of species traits has been identified as a key step to understand the associations of species in space (see Dormann et al. 2018). Bazzichetto et al. (2020) combine their GLM-based SDM for each species with a so-called multi-SDM approach, where they assess together the consistency in the interactions between both species and topographically-driven climate variations, and several plant traits and two key anthropic factors –accessibility from human settlements and distance to hiking paths.
This work is a good example on how a theoretically meaningful SDM approach can provide useful –though perhaps not deep– insights on biological invasions for remote landscapes threatened by biotic homogenization. By combining climate and topographic variables as proxies for the spatial variations in the abiotic conditions regulating plant growth, measures of accessibility, and traits of the plant invaders, Bazzichetto et al. (2020) are able to identify the different effects that the interactions between the potential intensity of propagule dissemination by humans, and the ecological characteristics of the invaders themselves, may have on their invasion success.
The innovation of modelling together species responses is important because it allows dissecting the spatial dynamics of spread of the invaders, which indeed vary according to a handful of their traits. For example, their results show that no all old residents have profited from the larger time of residence in the island, as Poa pratensis is seemingly as dependent of a higher intensity of human activity as the newcomer invaders in general are. According to Bazzichetto et al. trait-based analyses, these differences are apparently related with plant height, as smaller plants disperse more easily. Further, being perennial also provides an advantage for the persistence in areas with less human influence. This puts name, shame and fame to the known influence of plant life history on their dispersal success (Beckman et al. 2018), at least for the particular case of plant invasions in Possession Island.
Of course this approach has limitations, as data on the texture, chemistry and temperature of the soil are not available, and thus were not considered in the analyses. These factors may be critical for both establishment and persistence of small plants in the harsh Antarctic environments, as Bazzichetto et al. (2020) recognize. But all in all, their results provide key insights on which traits may confer alien plants with a higher likelihood of becoming successful invaders in the fragile Antarctic and sub-Antarctic ecosystems. This opens a way for rapid assessments of invasibility, which will help identifying which species in the process of naturalizing may require active contention measures to prevent them from becoming ecological game changers and cause disastrous cascade effects that shift the dynamics of native ecosystems.

References

Austin, M. P., Nicholls, A. O., and Margules, C. R. (1990). Measurement of the realized qualitative niche: environmental niches of five Eucalyptus species. Ecological Monographs, 60(2), 161-177. doi: https://doi.org/10.2307/1943043
Bazzichetto, M., Massol, F., Carboni, M., Lenoir, J., Lembrechts, J. J. and Joly, R. (2020) Once upon a time in the far south: Influence of local drivers and functional traits on plant invasion in the harsh sub-Antarctic islands. bioRxiv, 2020.07.19.210880, ver. 3 peer-reviewed and recommended by PCI Ecology. doi: https://doi.org/10.1101/2020.07.19.210880
Beckman, N. G., Bullock, J. M., and Salguero-Gómez, R. (2018). High dispersal ability is related to fast life-history strategies. Journal of Ecology, 106(4), 1349-1362. doi: https://doi.org/10.1111/1365-2745.12989
Croll, D. A., Maron, J. L., Estes, J. A., Danner, E. M., and Byrd, G. V. (2005). Introduced predators transform subarctic islands from grassland to tundra. Science, 307(5717), 1959-1961. doi: https://doi.org/10.1126/science.1108485
Dormann, C. F., Bobrowski, M., Dehling, D. M., Harris, D. J., Hartig, F., Lischke, H., Moretti, M. D., Pagel, J., Pinkert, S., Schleuning, M., Schmidt, S. I., Sheppard, C. S., Steinbauer, M. J., Zeuss, D., and Kraan, C. (2018). Biotic interactions in species distribution modelling: 10 questions to guide interpretation and avoid false conclusions. Global Ecology and Biogeography, 27(9), 1004-1016. doi: https://doi.org/10.1111/geb.12759
Jiménez-Valverde, A., Peterson, A., Soberón, J., Overton, J., Aragón, P., and Lobo, J. (2011). Use of niche models in invasive species risk assessments. Biological Invasions, 13(12), 2785-2797. doi: https://doi.org/10.1007/s10530-011-9963-4
Hortal, J., Lobo, J. M., and Jiménez-Valverde, A. (2012). Basic questions in biogeography and the (lack of) simplicity of species distributions: Putting species distribution models in the right place. Natureza & Conservação – Brazilian Journal of Nature Conservation, 10(2), 108-118. doi: https://doi.org/10.4322/natcon.2012.029
Hughes, K. A., Pertierra, L. R., Molina-Montenegro, M. A., and Convey, P. (2015). Biological invasions in terrestrial Antarctica: what is the current status and can we respond? Biodiversity and Conservation, 24(5), 1031-1055. doi: https://doi.org/10.1007/s10531-015-0896-6
Pertierra, L. R., Baker, M., Howard, C., Vega, G. C., Olalla-Tarraga, M. A., and Scott, J. (2016). Assessing the invasive risk of two non-native Agrostis species on sub-Antarctic Macquarie Island. Polar Biology, 39(12), 2361-2371. doi: https://doi.org/10.1007/s00300-016-1912-3
Pollock, L. J., Tingley, R., Morris, W. K., Golding, N., O'Hara, R. B., Parris, K. M., Vesk, P. A., and McCarthy, M. A. (2014). Understanding co-occurrence by modelling species simultaneously with a Joint Species Distribution Model (JSDM). Methods in Ecology and Evolution, 5(5), 397-406. doi: https://doi.org/10.1111/2041-210X.12180
Richardson, D. M., Pyšek, P., Rejmánek, M., Barbour, M. G., Panetta, F. D., and West, C. J. (2000). Naturalization and invasion of alien plants: concepts and definitions. Diversity and Distributions, 6(2), 93-107. doi: https://doi.org/10.1046/j.1472-4642.2000.00083.x

What kinds of studies are most needed to understand the effects of global change on nature? Two deficiencies stand out: lack of long-term studies [1] and lack of data on species interactions [2]. The paper by Mennerat and colleagues [3] is particularly valuable because it addresses both of these shortcomings. The first one is obvious. Our understanding of the impact of climate on biota improves with longer times series of observations. Mennerat et al. [3] analysed an impressive 18-year series from multiple sites to search for trends in parasitism rates across a range of temperatures. The second deficiency (lack of species interaction data) is perhaps not yet fully appreciated, despite studies pointing this out ten years ago [2,4]. The focus is often on species range limits and how taking species interactions into account changes species range predictions based on climate alone (climate envelope models; [5]). But range limits are not everything, as the function of a species (or community, network, etc.) ultimately depends on the strengths of species interactions and not only on the presence or absence of a given species [2,4]. Mennerat et al. [3] show that in the case of birds and their nest parasites, it is the strength of the interaction that has changed, while the species involved stayed the same. Mennerat et al. [3] found nest parasitism to increase with temperature at the nestling stage. They have also searched for trends of parasitism dynamics dependence on the host, but did not find any, probably because the nest parasites are generalists and attack other bird species within the study sites. This study thus draws attention to wider networks of interacting species, and we urgently need more data to predict how interaction networks will rewire with progressing environmental change [6,7].

References

[1] Lindenmayer, D.B., Likens, G.E., Andersen, A., Bowman, D., Bull, C.M., Burns, E., et al. (2012). Value of long-term ecological studies. Austral Ecology, 37(7), 745–57. doi: 10.1111/j.1442-9993.2011.02351.x
[2] Tylianakis, J.M., Didham, R.K., Bascompte, J. & Wardle, D.A. (2008). Global change and species interactions in terrestrial ecosystems. Ecology Letters, 11(12), 1351–63. doi: 10.1111/j.1461-0248.2008.01250.x
[3] Mennerat, A., Charmantier, A., Hurtrez-Bousses, S., Perret, P. & Lambrechts, M.M. (2019). Parasite intensity is driven by temperature in a wild bird. bioRxiv, 323311. Ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/323311
[4] Gilman, S.E., Urban, M.C., Tewksbury, J., Gilchrist, G.W. & Holt, R.D. (2010). A framework for community interactions under climate change. Trends in Ecology & Evolution, 25(6), 325–31. doi: 10.1016/j.tree.2010.03.002
[5] Louthan, A.M., Doak, D.F. & Angert, A.L. (2015). Where and when do species interactions set range limits? Trends in Ecology & Evolution, 30(12), 780–92. doi: 10.1016/j.tree.2015.09.011
[6] Bartley, T.J., McCann, K.S., Bieg, C., Cazelles, K., Granados, M., Guzzo, M.M., et al. (2019). Food web rewiring in a changing world. Nature Ecology & Evolution, 3(3), 345–54. doi: 10.1038/s41559-018-0772-3
[7] Staniczenko, P.P.A., Lewis, O.T., Jones, N.S. & Reed-Tsochas, F. (2010). Structural dynamics and robustness of food webs. Ecology Letters, 13(7), 891–9. doi: 10.1111/j.1461-0248.2010.01485.x

Rodents are well known as one of the main animal groups responsible for human-transmitted pathogens. As such, it seems logical to try and survey what kinds of pathogenic microbes might be harboured by wild rodents, in order to establish some baseline surveillance and prevent future zoonotic outbreaks (Bernstein et al., 2022). This is exactly what Abbate et al. (2023) endeavoured and their findings are intimidating. Based on quite a large sampling effort, they collected more than 700 rodents of seven species around two villages in northeastern France. They looked for molecular markers indicative of viral and bacterial infections and proceeded to analyze their pathogen communities using multivariate techniques.

Variation in the prevalence of the different pathogens was found among host species, with e.g. signs of CPXV more prevalent in Cricetidae while some Mycoplasma strains were more prevalent in Muridae. Co-circulation of pathogens was found in all species, with some evidencing signs of up to 12 different pathogen taxa. The diversity of co-circulating pathogens was markedly different between host species and higher in adult hosts, but not affected by sex. The dataset also evinced some slight differences between habitats, with meadows harbouring a little more diversity of rodent pathogens than forests. Less intuitively, some pathogen associations seemed quite repeatable, such as the positive association of Bartonella spp. with CPXV in the montane water vole. The study allowed the authors to test several associations already described in the literature, including associations between different hemotropic Mycoplasma species.

I strongly invite colleagues interested in zoonoses, emerging pandemics and more generally One Health to read the paper of Abbate et al. (2023) and try to replicate them across the world. To prevent the next sanitary crises, monitoring rodents, and more generally vertebrates, population demographics is a necessary and enlightening step (Johnson et al., 2020), but insufficient. Following the lead of colleagues working on rodent ectoparasites (Krasnov et al., 2014), we need more surveys like the one described by Abbate et al. (2023) to understand the importance of the dilution effect in the prevalence and transmission of microbial pathogens (Andreazzi et al., 2023) and the formation of epidemics. We also need other similar studies to assess the potential of different rodent species to carry pathogens more or less capable of infecting other mammalian species (Morand et al., 2015), in other places in the world.

References

Abbate, J. L., Galan, M., Razzauti, M., Sironen, T., Voutilainen, L., Henttonen, H., Gasqui, P., Cosson, J.-F. & Charbonnel, N. (2023) Pathogen community composition and co-infection patterns in a wild community of rodents. BioRxiv, ver.4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2020.02.09.940494 

Andreazzi, C. S., Martinez-Vaquero, L. A., Winck, G. R., Cardoso, T. S., Teixeira, B. R., Xavier, S. C. C., Gentile, R., Jansen, A. M. & D'Andrea, P. S. (2023) Vegetation cover and biodiversity reduce parasite infection in wild hosts across ecological levels and scales. Ecography, 2023, e06579.
https://doi.org/10.1111/ecog.06579
 
Bernstein, A. S., Ando, A. W., Loch-Temzelides, T., Vale, M. M., Li, B. V., Li, H., Busch, J., Chapman, C. A., Kinnaird, M., Nowak, K., Castro, M. C., Zambrana-Torrelio, C., Ahumada, J. A., Xiao, L., Roehrdanz, P., Kaufman, L., Hannah, L., Daszak, P., Pimm, S. L. & Dobson, A. P. (2022) The costs and benefits of primary prevention of zoonotic pandemics. Science Advances, 8, eabl4183.
https://doi.org/10.1126/sciadv.abl4183
 
Johnson, C. K., Hitchens, P. L., Pandit, P. S., Rushmore, J., Evans, T. S., Young, C. C. W. & Doyle, M. M. (2020) Global shifts in mammalian population trends reveal key predictors of virus spillover risk. Proceedings of the Royal Society B: Biological Sciences, 287, 20192736.
https://doi.org/10.1098/rspb.2019.2736
 
Krasnov, B. R., Pilosof, S., Stanko, M., Morand, S., Korallo-Vinarskaya, N. P., Vinarski, M. V. & Poulin, R. (2014) Co-occurrence and phylogenetic distance in communities of mammalian ectoparasites: limiting similarity versus environmental filtering. Oikos, 123, 63-70.
https://doi.org/10.1111/j.1600-0706.2013.00646.x
 
Morand, S., Bordes, F., Chen, H.-W., Claude, J., Cosson, J.-F., Galan, M., Czirjak, G. Á., Greenwood, A. D., Latinne, A., Michaux, J. & Ribas, A. (2015) Global parasite and Rattus rodent invasions: The consequences for rodent-borne diseases. Integrative Zoology, 10, 409-423.
https://doi.org/10.1111/1749-4877.12143

"Good and evil are so close as to be chained together in the soul"
Robert Louis Stevenson, Dr. Jekyll and Mr. Hyde

Maternally inherited symbionts—microorganisms that pass from a female host to her progeny—have two main ways of increasing their own fitness. First, they can increase the fecundity or viability of infected females. This “positive fitness effects” strategy is the one commonly used by mutualistic symbionts, such as Buchnera aphidicola—the bacterial endosymbiont of the pea aphid, Acyrthosiphon pisum [4]. Second, maternally inherited symbionts can manipulate the reproduction of infected females in a way that enhances symbiont transmission at the expense of host fitness. A famous example of this “reproductive parasitism” strategy is the cytoplasmic incompatibility (CI) [3] induced by bacteria of the genus Wolbachia in their arthropod and nematode hosts. CI works as a toxin-antidote system, whereby the sperm of infected males is modified in a lethal way (toxin) that can only be reverted if the egg is also infected (antidote) [1]. As a result, CI imposes a kind of conditional sterility on their hosts: while infected females are compatible with both infected and uninfected males, uninfected females experience high offspring mortality if (and only if) they mate with infected males [7].

These two symbiont strategies (positive fitness effects versus reproductive parasitism) have been traditionally studied separately, both empirically and theoretically. However, it has become clear that the two strategies are not mutually exclusive, and that a reproductive parasite can simultaneously act as a mutualist—an infection type that has been dubbed “Jekyll and Hyde” [6], after the famous novella by Robert Louis Stevenson about kind scientist Dr. Jekyll and his evil alter ego, Mr. Hyde. In important previous work, Zug and Hammerstein [7] analyzed the consequences of positive fitness effects on the dynamics of different kind of infections, including “Jekyll and Hyde” infections characterized by CI and other reproductive parasitism strategies. Building on this and related modeling framework, Karisto et al. [2] re-investigate and expand on the interplay between positive fitness effects and reproductive parasitism in Wolbachia infections by focusing on CI in both diplodiploid and haplodiploid populations, and by paying particular attention to the mathematical assumption structure underlying their results.

Karisto et al. begin by reviewing classic models of Wolbachia infections in diplodiploid populations that assume a “negative fitness effect” (modeled as a fertility penalty on infected females), characteristic of a pure strategy of reproductive parasitism. Together with the positive frequency-dependent effects due to CI (whereby the fitness benefits to symbionts infecting females increase with the proportion of infected males in the population) this results in population dynamics characterized by two stable equilibria (the Wolbachia-free state and an interior equilibrium with a high frequency of Wolbachia-carrying hosts) separated by an unstable interior equilibrium. Wolbachia can then spread once the initial frequency is above a threshold or an invasion barrier, but is prevented from fixing by a proportion of infections failing to be passed on to offspring. Karisto et al. show that, given the assumption of negative fitness effects, the stable interior equilibrium can never feature a Wolbachia prevalence below one-half. Moreover, they convincingly argue that a prevalence greater than but close to one-half is difficult to maintain in the presence of stochastic fluctuations, as in these cases the high-prevalence stable equilibrium would be too close to the unstable equilibrium signposting the invasion barrier.

Karisto et al. then relax the assumption of negative fitness effects and allow for positive fitness effects (modeled as a fertility premium on infected females) in a diplodiploid population. They show that positive fitness effects may result in situations where the original invasion threshold is now absent, the bistable coexistence dynamics are transformed into purely co-existence dynamics, and Wolbachia symbionts can now invade when rare. Karisto et al. conclude that positive fitness effects provide a plausible and potentially testable explanation for the low frequencies of symbiont-carrying hosts that are sometimes observed in nature, which are difficult to reconcile with the assumption of negative fitness effects. 

Finally, Karisto et al. extend their analysis to haplodiploid host populations (where all fertilized eggs develop as females). Here, they investigate two types of cytoplasmic incompatibility: a female-killing effect, similar to the CI effect studied in diplodiploid populations (the “Leptopilina type” of Vavre et al. [5]) and a masculinization effect, where CI leads to the loss of paternal chromosomes and to the development of the offspring as a male (the “Nasonia type” of Vavre et al. [5]). The models are now two-sex, which precludes a complete analytical treatment, in particular regarding the stability of fixed points. Karisto et al. compensate by conducting large numerical analyses that support their claims. Importantly, all main conclusions regarding the interplay between positive fitness effects and reproductive parasitism continue to hold under haplodiploidy. 

All in all, the analysis and results by Karisto et al. suggest that it is not necessary to resort to classical (but depending on the situation, unlikely) mechanisms, such as ongoing invasion or source-sink dynamics, to explain arthropod populations featuring low-prevalent Wolbachia infections. Instead, low-frequency equilibria might be simply due to reproductive parasites conferring beneficial fitness effects, or Wolbachia symbionts playing Dr. Jekyll (positive fitness effects) and Mr. Hyde (cytoplasmatic incompatibility). 

References

[1] Beckmann JF, Bonneau M, Chen H, Hochstrasser M, Poinsot D, Merçot H, Weill M, Sicard M, Charlat S (2019) The Toxin–Antidote Model of Cytoplasmic Incompatibility: Genetics and Evolutionary Implications. Trends in Genetics, 35, 175–185. https://doi.org/10.1016/j.tig.2018.12.004

[2] Karisto P, Duplouy A, Vries C de, Kokko H (2022) Positive fitness effects help explain the broad range of Wolbachia prevalences in natural populations. bioRxiv, 2022.04.11.487824, ver. 5 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.04.11.487824

[3] Laven H (1956) Cytoplasmic Inheritance in Culex. Nature, 177, 141–142. https://doi.org/10.1038/177141a0

[4] Perreau J, Zhang B, Maeda GP, Kirkpatrick M, Moran NA (2021) Strong within-host selection in a maternally inherited obligate symbiont: Buchnera and aphids. Proceedings of the National Academy of Sciences, 118, e2102467118. https://doi.org/10.1073/pnas.2102467118

[5] Vavre F, Fleury F, Varaldi J, Fouillet P, Bouletreau M (2000) Evidence for Female Mortality in Wolbachia-Mediated Cytoplasmic Incompatibility in Haplodiploid Insects: Epidemiologic and Evolutionary Consequences. Evolution, 54, 191–200. https://doi.org/10.1111/j.0014-3820.2000.tb00019.x

[6] Zug R, Hammerstein P (2015) Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts. Biological Reviews, 90, 89–111. https://doi.org/10.1111/brv.12098

[7] Zug R, Hammerstein P (2018) Evolution of reproductive parasites with direct fitness benefits. Heredity, 120, 266–281. https://doi.org/10.1038/s41437-017-0022-5

Michael Raatz (2023) provides here a relevant exploration of higher-order interactions, i.e. interactions involving more than two related species (Terry et al. 2019), in the case of food web and competition interactions. More precisely, he shows by modeling that essential resources may significantly mediate focal species' persistence. Simultaneously, the provision of essential resources may strongly affect the resulting community structure, by driving to extinction first the predator and then, depending on the higher-order interaction, potentially also the associated competitor. 

Today, all ecologists should be aware of the potential effects of high-order interactions on species' (and likely on ecosystem's) fate (Golubski et al. 2016, Grilli et al. 2017). Yet, we should soon be prepared to include any high-order interaction into any interaction network (i.e. not only between species, but also between species and abiotic components, and between biotic, anthropogenic and abiotic components too). For this purpose, we will need innovative approaches such as hypergraphs (Golubski et al. 2016) and discrete-event models (Gaucherel and Pommereau 2019, Thomas et al. 2022) able to manage highly complex interactions, with numerous interacting components and variables. Such a rigorous study is a necessary and preliminary step in taking into account such a higher complexity. 

References

Gaucherel, C. and F. Pommereau. 2019. Using discrete systems to exhaustively characterize the dynamics of an integrated ecosystem. Methods in Ecology and Evolution 00:1–13. https://doi.org/10.1111/2041-210X.13242

Golubski, A. J., E. E. Westlund, J. Vandermeer, and M. Pascual. 2016. Ecological Networks over the Edge: Hypergraph Trait-Mediated Indirect Interaction (TMII) Structure trends in Ecology & Evolution 31:344-354. https://doi.org/10.1016/j.tree.2016.02.006

Grilli, J., G. Barabas, M. J. Michalska-Smith, and S. Allesina. 2017. Higher-order interactions stabilize dynamics in competitive network models. Nature 548:210-213. https://doi.org/10.1038/nature23273

Raatz, M. 2023. Provision of essential resources as a persistence strategy in food webs. bioRxiv, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2023.01.27.525839

Terry, J. C. D., R. J. Morris, and M. B. Bonsall. 2019. Interaction modifications lead to greater robustness than pairwise non-trophic effects in food webs. Journal of Animal Ecology 88:1732-1742. https://doi.org/10.1111/1365-2656.13057

Thomas, C., M. Cosme, C. Gaucherel, and F. Pommereau. 2022. Model-checking ecological state-transition graphs. PLoS Computational Biology 18:e1009657. https://doi.org/10.1371/journal.pcbi.1009657