Direct and transgenerational effects of an experimental heat wave on early life stages in a freshwater snail
Katja Leicht, Otto Seppälä
https://doi.org/10.1101/449777
Escargots cooked just right: telling apart the direct and indirect effects of heat waves in freashwater snails
Recommended by vincent calcagno based on reviews by Amanda Lynn Caskenette, Kévin Tougeron and arnaud sentis
Amongst the many challenges and forms of environmental change that organisms face in our era of global change, climate change is perhaps one of the most straightforward and amenable to investigation. First, measurements of day-to-day temperatures are relatively feasible and accessible, and predictions regarding the expected trends in Earth surface temperature are probably some of the most reliable we have. It appears quite clear, in particular, that beyond the overall increase in average temperature, the heat waves locally experienced by organisms in their natural habitats are bound to become more frequent, more intense, and more long-lasting [1]. Second, it is well appreciated that temperature is a major environmental factor with strong impacts on different facets of organismal development and life-history [2-4]. These impacts have reasonably clear mechanistic underpinnings, with definite connections to biochemistry, physiology, and considerations on energetics. Third, since variation in temperature is a challenge already experienced by natural populations across their current and historical ranges, it is not a completely alien form of environmental change. Therefore, we already learnt quite a lot about it in several species, and so did the species, as they may be expected to have evolved dedicated adaptive mechanisms to respond to elevated temperatures. Last, but not least, temperature is quite amenable to being manipulated as an experimental factor.
For all these reasons, experimental studies of the consequences of increased temperature hit some of a sweetspot and are a source of very nice research, in many different organisms. The work by Leicht and Seppala [5] complements a sequence of earlier studies by this group, using the freshwater snail Lymnaea stagnalis as their model system [6-7].
In the present study, the authors investigate how a heat wave (a period of abnormally elevated temperature, here 25°C versus a normal 15°C) may have indirect effects on the next generation, through maternal effects. They question whether such indirect effects exist, and if they exist, how they compare, in terms of effect size, with the (more straightforward) direct effects observed in individuals that directly experience a heat wave. Transgenerational effects are well-known to occur following periods of physiological stress, and might thus have non negligible contributions to the overall effect of warming.
In this freshwater snail, heat has very strong direct effects: mortality increases at high temperature, but survivors grow much bigger, with a greater propensity to lay eggs and a (spectacular) three-fold increase in the number of eggs laid [6]. Considering that, it is easy to consider that transgenerational effects should be small game. And indeed, the present study also observes the big and obvious direct effects of elevated temperature: higher mortality, but greater propensity to oviposit. However, it was also found that the eggs were smaller if from mothers exposed to high temperature, with a correspondingly smaller size of hatchlings. This suggests that a heat wave causes the snails to lay more eggs, but smaller ones, reminiscent of a size-number trade-off. Unfortunately, clutch size could not be measured in this experiment, so this cannot be investigated any further. For this trait, the indirect effect may indeed be regarded as small game : eggs and hatchlings were about 15 % smaller, an effect size pretty small compared to the mammoth direct positive effect of temperature on shell length (see Figure 4 ; and also [6]). The same is true for developmental time (Figure 3).
However, for some traits the story was different. In particular, it was found that the (smaller) eggs produced from heated mothers were more likely to hatch by almost 10% (Figure 2). Here the indirect effect not only goes against the direct effect (hatching rate is lower at high temperature), but it also has similar effect size. As a consequence, taking into account both the indirect and direct effects, hatching success is essentially the same at 15°C and 25°C (Figure 2). Survival also had comparable effect sizes for direct and indirect effects. Indeed, survival was reduced by about 20% regardless of whom endured the heat stress (the focal individual or her mother; Figure 4). Interestingly, the direct and indirect effects were not quite cumulative: if a mother experienced a heat wave, heating up the offspring did not do much more damage, as though the offspring were ‘adapted’ to the warmer conditions (but keep in mind that, surprisingly, the authors’ stats did not find a significant interaction; Table 2).
At the end of the day, even though at first heat seems a relatively simple and understandable component of environmental change, this study shows how varied its effects can be effects on different components of individual fitness. The overall impact most likely is a mix of direct and indirect effects, of shifts along allocation trade-offs, and of maladaptive and adaptive responses, whose overall ecological significance is not so easy to grasp. That said, this study shows that direct and indirect (maternal) effects can sometimes go against one another and have similar intensities. Indirect effects should therefore not be overlooked in this kind of studies. It also gives a hint of what an interesting challenge it is to understand the adaptive or maladaptive nature of organism responses to elevated temperatures, and to evaluate their ultimate fitness consequences.
References
[1] Meehl, G. A., & Tebaldi, C. (2004). More intense, more frequent, and longer lasting heat waves in the 21st century. Science (New York, N.Y.), 305(5686), 994–997. doi: 10.1126/science.1098704
[2] Adamo, S. A., & Lovett, M. M. E. (2011). Some like it hot: the effects of climate change on reproduction, immune function and disease resistance in the cricket Gryllus texensis. The Journal of Experimental Biology, 214(Pt 12), 1997–2004. doi: 10.1242/jeb.056531
[3] Deutsch, C. A., Tewksbury, J. J., Tigchelaar, M., Battisti, D. S., Merrill, S. C., Huey, R. B., & Naylor, R. L. (2018). Increase in crop losses to insect pests in a warming climate. Science (New York, N.Y.), 361(6405), 916–919. doi: 10.1126/science.aat3466
[4] Sentis, A., Hemptinne, J.-L., & Brodeur, J. (2013). Effects of simulated heat waves on an experimental plant–herbivore–predator food chain. Global Change Biology, 19(3), 833–842. doi: 10.1111/gcb.12094
[5] Leicht, K., & Seppälä, O. (2019). Direct and transgenerational effects of an experimental heat wave on early life stages in a freshwater snail. BioRxiv, 449777, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/449777
[6] Leicht, K., Seppälä, K., & Seppälä, O. (2017). Potential for adaptation to climate change: family-level variation in fitness-related traits and their responses to heat waves in a snail population. BMC Evolutionary Biology, 17(1), 140. doi: 10.1186/s12862-017-0988-x
[7] Leicht, K., Jokela, J., & Seppälä, O. (2013). An experimental heat wave changes immune defense and life history traits in a freshwater snail. Ecology and Evolution, 3(15), 4861–4871. doi: 10.1002/ece3.874
| Direct and transgenerational effects of an experimental heat wave on early life stages in a freshwater snail | Katja Leicht, Otto Seppälä | <p>Global climate change imposes a serious threat to natural populations of many species. Estimates of the effects of climate change‐mediated environmental stresses are, however, often based only on their direct effects on organisms, and neglect t... |  | Climate change | vincent calcagno | | 2018-10-22 22:19:22 | View |
Probing behaviors correlated with behavioral flexibility
Recommended by Jeremy Van Cleve based on reviews by 2 anonymous reviewers
Behavioral plasticity, which is a subset of phenotypic plasticity, is an important component of foraging, defense against predators, mating, and many other behaviors. More specifically, behavioral flexibility, in this study, captures how quickly individuals adapt to new circumstances. In cases where individuals disperse to new environments, which often occurs in range expansions, behavioral flexibility is likely crucial to the chance that individuals can establish in these environments. Thus, it is important to understand how best to measure behavioral flexibility and how measures of such flexibility might vary across individuals and behavioral contexts and with other measures of learning and problem solving.
In this preregistration, Logan and colleagues propose to use a long-term study of the great-tailed grackle to measure how much they can manipulate behavioral flexibility in a reversal learning task, how much behavioral flexibility in one task predicts flexibility in another task and in problem solving a new task, and how robust these patterns are within individuals and across tasks. Logan and colleagues lay out their hypotheses and predictions for each experiment in a clear and concise manner. They also are very clear about the details of their study system, such as how they determined the number of trials they use in their learning reversal experiments, and how those details have influenced their experimental design. Further, given that the preregistration uses RMarkdown and is stored on GitHub (as are other studies in the larger project), their statistical code and its history of modification are easily available. This is a crucial component of making research more reproducible, which is a recent emphasis in behavioral sciences more broadly.
Reviewers of this preregistration found the study of substantial merit. The authors have responded to the reviewers' comments and their revisions have made the preregistration much clearer and cogent. I am happy to recommend this preregistration.
| Is behavioral flexibility linked with exploration, but not boldness, persistence, or motor diversity? | Kelsey McCune, Carolyn Rowney, Luisa Bergeron, Corina Logan | This is a PREREGISTRATION. The DOI was issued by OSF and refers to the whole GitHub repository, which contains multiple files. The specific file we are submitting is g_exploration.Rmd, which is easily accessible at GitHub at https://github.com/cor... |  | Behaviour & Ethology, Preregistrations, Zoology | Jeremy Van Cleve | | 2018-09-27 03:35:12 | View |
Is behavioral flexibility manipulatable and, if so, does it improve flexibility and problem solving in a new context?
Corina Logan, Carolyn Rowney, Luisa Bergeron, Benjamin Seitz, Aaron Blaisdell, Zoe Johnson-Ulrich, Kelsey McCune
http://corinalogan.com/Preregistrations/g_flexmanip.html
Can context changes improve behavioral flexibility? Towards a better understanding of species adaptability to environmental changes
Recommended by Aurélie Coulon based on reviews by Maxime Dahirel and Andrea Griffin
Behavioral flexibility is a key for species adaptation to new environments. Predicting species responses to new contexts hence requires knowledge on the amount to and conditions in which behavior can be flexible. This is what Logan and collaborators propose to assess in a series of experiments on the great-tailed grackles, in a context of rapid range expansion. This pre-registration is integrated into this large research project and concerns more specifically the manipulability of the cognitive aspects of behavioral flexibility. Logan and collaborators will use reversal learning tests to test whether (i) behavioral flexibility is manipulatable, (ii) manipulating flexibility improves flexibility and problem solving in a new context, (iii) flexibility is repeatable within individuals, (iv) individuals are faster at problem solving as they progress through serial reversals. The pre-registration carefully details the hypotheses, their associated predictions and alternatives, and the plan of statistical analyses, including power tests. The ambitious program presented in this pre-registration has the potential to provide important pieces to better understand the mechanisms of species adaptability to new environments.
| Is behavioral flexibility manipulatable and, if so, does it improve flexibility and problem solving in a new context? | Corina Logan, Carolyn Rowney, Luisa Bergeron, Benjamin Seitz, Aaron Blaisdell, Zoe Johnson-Ulrich, Kelsey McCune | This is one of the first studies planned for our long-term research on the role of behavioral flexibility in rapid geographic range expansions. Behavioral flexibility, the ability to adapt behavior to new circumstances, is thought to play an impor... |  | Behaviour & Ethology, Preregistrations, Zoology | Aurélie Coulon | | 2018-07-03 13:23:10 | View |
Evaluating functional dispersal and its eco-epidemiological implications in a nest ectoparasite
Amalia Rataud, Marlène Dupraz, Céline Toty, Thomas Blanchon, Marion Vittecoq, Rémi Choquet, Karen D. McCoy
https://doi.org/10.5281/zenodo.2592114
Limited dispersal in a vector on territorial hosts
Recommended by Adele Mennerat based on reviews by Shelly Lachish and 1 anonymous reviewer
Parasitism requires parasites and hosts to meet and is therefore conditioned by their respective dispersal abilities. While dispersal has been studied in a number of wild vertebrates (including in relation to infection risk), we still have poor knowledge of the movements of their parasites. Yet we know that many parasites, and in particular vectors transmitting pathogens from host to host, possess the ability to move actively during at least part of their lives.
So... how far does a vector go – and is this reflected in the population structure of the pathogens they transmit? This is the question addressed by Rataud et al. [1], who provide the first attempt at using capture-mark-recapture to estimate not only functional dispersal, but also detection probability and survival in a wild parasite that is also a vector for other pathogens.
The authors find that (i) functional dispersal of soft ticks within a gull colony is very limited. Moreover, they observe unexpected patterns: (ii) experimental displacement of ticks does not induce homing behaviour, and (iii) despite lower survival, tick dispersal was lower in nests not containing hosts than in successful nests.
These results contrast with expectations based on the distribution of infectious agents. Low tick dispersal within the colony, combined with host territoriality during breeding and high site fidelity between years should result in a spatially structured distribution of infectious agents carried by ticks. This is not the case here. One possible explanation could be that soft ticks live for much longer than a breeding season, and that they disperse at other times of year to a larger extent than usually assumed.
This study represents one chapter of a story that will likely keep unfolding. It raises fascinating questions, and illustrates the importance of basic knowledge of parasite ecology and behaviour to better understand pathogen dynamics in the wild.
References
[1] Rataud A., Dupraz M., Toty C., Blanchon T., Vittecoq M., Choquet R. & McCoy K.D. (2019). Evaluating functional dispersal and its eco-epidemiological implications in a nest ectoparasite. Zenodo, 2592114. Ver. 3 peer-reviewed and recommended by PCI Ecology. doi: 10.5281/zenodo.2592114
| Evaluating functional dispersal and its eco-epidemiological implications in a nest ectoparasite | Amalia Rataud, Marlène Dupraz, Céline Toty, Thomas Blanchon, Marion Vittecoq, Rémi Choquet, Karen D. McCoy | <p>Functional dispersal (between-site movement, with or without subsequent reproduction) is a key trait acting on the ecological and evolutionary trajectories of a species, with potential cascading effects on other members of the local community. ... |  | Dispersal & Migration, Epidemiology, Parasitology, Population ecology | Adele Mennerat | | 2018-11-05 11:44:58 | View |
Adapting to a changing environment: advancing our understanding of the mechanisms that lead to behavioral flexibility
Recommended by Erin Vogel based on reviews by Simon Gingins and 2 anonymous reviewers
Behavioral flexibility is essential for organisms to adapt to an ever-changing environment. However, the mechanisms that lead to behavioral flexibility and understanding what traits makes a species better able to adapt behavior to new environments has been understudied. Logan and colleagues have proposed to use a series of experiments, using great-tailed grackles as a study species, to test four main hypotheses. These hypotheses are centered around exploring the relationship between behavioral flexibility and inhibition in grackles. This current preregistration is a part of a larger integrative research plan examining behavioral flexibility when faced with environmental change. In this part of the project they will examine specifically if individuals that are more flexible are also better at inhibiting: in other words: they will test the assumption that inhibition is required for flexibility.
First, they will test the hypothesis that behavioral flexibility is manipulatable by using a serial reversal learning task. Second, they will test the hypothesis that manipulating behavioral flexibility (improving reversal learning speed through serial reversals using colored tubers) improves flexibility (rule switching) and problem solving in a new context (multi‑access box and serial reversals on a touch screen). Third, they will test the hypothesis that behavioral flexibility within a context is repeatable within individuals, which is important to test if performance is state dependent. Finally, they will test a fourth hypothesis that individuals should converge on an epsilon‑first learning strategy (learn the correct choice after one trial) as they progress through serial reversals. Their innovative approach using three main tasks (delay of gratification, go-no, detour) will allow them to assess different aspects of inhibitory control. They will analyze the results of all three experiments to also assess the utility of these experiments for studying the potential relationship between inhibition and behavioral flexibility.
In their preregistration, Logan and colleagues have proposed to test these hypotheses, each with a set of testable predictions that can be examined with detailed and justified methodologies. They have also provided a comprehensive plan for analyzing the data. All of the reviewers and I agree that this is a very interesting study that has the potential to answer important questions about a critical topic in behavioral ecology: the role of inhibition in the evolution of behavioral flexibility. Given the positive reviews, the comprehensive responses by the PI and her colleagues, and careful revisions, I highly recommend this preregistration.
| Are the more flexible great-tailed grackles also better at inhibition? | Corina Logan, Kelsey McCune, Zoe Johnson-Ulrich, Luisa Bergeron, Carolyn Rowney, Benjamin Seitz, Aaron Blaisdell, Claudia Wascher | This is a PREREGISTRATION. The DOI was issued by OSF and refers to the whole GitHub repository, which contains multiple files. The specific file we are submitting is g_inhibition.Rmd, which is easily accessible at GitHub at https://github.com/cori... |  | Behaviour & Ethology, Preregistrations, Zoology | Erin Vogel | | 2018-10-12 18:36:00 | View |
Parasite intensity is driven by temperature in a wild bird
Adèle Mennerat, Anne Charmantier, Sylvie Hurtrez-Boussès, Philippe Perret, Marcel M Lambrechts
https://doi.org/10.1101/323311
The global change of species interactions
Recommended by Jan Hrcek based on reviews by 2 anonymous reviewers
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
| Parasite intensity is driven by temperature in a wild bird | Adèle Mennerat, Anne Charmantier, Sylvie Hurtrez-Boussès, Philippe Perret, Marcel M Lambrechts | <p>Increasing awareness that parasitism is an essential component of nearly all aspects of ecosystem functioning, as well as a driver of biodiversity, has led to rising interest in the consequences of climate change in terms of parasitism and dise... |  | Climate change, Evolutionary ecology, Host-parasite interactions, Parasitology, Zoology | Jan Hrcek | | 2018-05-17 14:37:14 | View |
Photosynthesis of Laminaria digitata during the immersion and emersion periods of spring tidal cycles during hot, sunny weather
Aline Migné, Gaspard Delebecq, Dominique Davoult, Nicolas Spilmont, Dominique Menu, Marie-Andrée Janquin and François Gévaert
https://hal.sorbonne-universite.fr/hal-01827565v4
Evaluating physiological responses of a kelp to environmental changes at its vulnerable equatorward range limit
Recommended by Matthew Bracken based on reviews by 2 anonymous reviewers
Understanding processes at species’ range limits is of paramount importance in an era of global change. For example, the boreal kelp Laminaria digitata, which dominates low intertidal and shallow subtidal rocky reefs in northwestern Europe, is declining in the equatorward portion of its range [1]. In this contribution, Migné and colleagues [2] focus on L. digitata near its southern range limit on the coast of France and use a variety of techniques to paint a complete picture of the physiological responses of the kelp to environmental changes. Importantly, and in contrast to earlier work on the species which focused on subtidal individuals (e.g. [3]), Migné et al. [2] describe responses not only in the most physiologically stressful portion of the species’ range but also in the most stressful portion of its local environment: the upper portion of its zone on the shoreline, where it is periodically exposed to aerial conditions and associated thermal and desiccation stresses.
The authors show that whereas L. digitata possesses mechanisms to protect it from irradiance stress at low tide, these mechanisms are not sufficient to prevent damage to photosynthetic pathways (e.g., reduction in optimal quantum yields of photosystem II). This species experiences severe heat stress associated with mid-day low tides during the summer, and the cumulative damage associated with these stresses is likely associated with the range contraction that is currently underway. Given the important role that L. digitata plays as food and habitat for other organisms, its loss will have cascading impacts on community structure and ecosystem functioning. Understanding the mechanisms underlying these declines is essential to understanding the impacts of climate change on species, communities, and ecosystems.
References
[1] Raybaud, V., Beaugrand, G., Goberville, E., Delebecq, G., Destombe, C., Valero, M., Davoult, D., Morin, P. & Gevaert, F. (2013). Decline in kelp in west Europe and climate. PloS one, 8(6), e66044. doi: 10.1371/journal.pone.0066044
[2] Delebecq, G., Davoult, D., Menu, D., Janquin, M. A., Migné, A., Dauvin, J. C., & Gevaert, F. (2011). In situ photosynthetic performance of Laminaria digitata (Phaeophyceae) during spring tides in Northern Brittany. CBM-Cahiers de Biologie Marine, 52(4), 405. doi: 10.21411/CBM.A.C9EE91F
[3] Migné, A., Delebecq, G., Davoult, D., Spilmont, N., Menu, D., Janquin, M.-A., and Gevaert, F. (2019). Photosynthesis of Laminaria digitata during the immersion and emersion periods of spring tidal cycles during hot, sunny weather. Hal, 01827565, ver. 4 peer-reviewed and recommended by PCI Ecology. hal-01827565
| Photosynthesis of Laminaria digitata during the immersion and emersion periods of spring tidal cycles during hot, sunny weather | Aline Migné, Gaspard Delebecq, Dominique Davoult, Nicolas Spilmont, Dominique Menu, Marie-Andrée Janquin and François Gévaert | The boreal kelp Laminaria digitata dominates the low intertidal and upper subtidal zones of moderately exposed rocky shores in north-western Europe. Due to ocean warming, this foundation species is predicted to disappear from French coasts in the ... |  | Marine ecology | Matthew Bracken | | 2018-07-02 18:03:11 | View |
Differential immune gene expression associated with contemporary range expansion of two invasive rodents in Senegal
Nathalie Charbonnel, Maxime Galan, Caroline Tatard, Anne Loiseau, Christophe Diagne, Ambroise Dalecky, Hugues Parrinello, Stephanie Rialle, Dany Severac and Carine Brouat
https://doi.org/10.1101/442160
Are all the roads leading to Rome?
Recommended by Simon Blanchet based on reviews by Nadia Aubin-Horth and 1 anonymous reviewer
Identifying the factors which favour the establishment and spread of non-native species in novel environments is one of the keys to predict - and hence prevent or control - biological invasions. This includes biological factors (i.e. factors associated with the invasive species themselves), and one of the prevailing hypotheses is that some species traits may explain their impressive success to establish and spread in novel environments [1]. In animals, most research studies have focused on traits associated with fecundity, age at maturity, level of affiliation to humans or dispersal ability for instance. The “composite picture” of the perfect (i.e. successful) invader that has gradually emerged is a small-bodied animal strongly affiliated to human activities with high fecundity, high dispersal ability and a super high level of plasticity. Of course, the story is not that simple, and actually a perfect invader sometimes – if not often- takes another form… Carrying on to identify what makes a species a successful invader or not is hence still an important research axis with major implications.
In this manuscript, Charbonnel and collaborators [2] provide an interesting opportunity to gain novel insights into our understanding of (the) traits underlying invasion success. They nicely combine the power of Next-Generation Sequencing (NGS) with a clever comparative approach of two closely-related invasive rodents (the house mouse Mus musculus and the black rat Rattus rattus) in a common environment. They use this experimental design to test the appealing hypothesis that pathogens may be actors of the story, and may indirectly explain why some non-native species are so successful in invading novel habitats.
It is generally assumed that the community of pathogens encountered by non-native species in novel environments is different from that of their native area. On the one hand (the enemy-release hypothesis), it can be hypothesized that non-native species, when they arrive into a novel environment, will be relaxed from the pressure imposed by their native pathogens because local pathogens are not adapted (and hence do not infect) to this novel host. Because immune defence against pathogens is highly costly, non-native species establishing into a novel environment could hence reallocate these costs to other functions such as fecundity or dispersal apparatus. This scenario has been termed the “evolution of increased competitive ability” (EICA) hypothesis [3]. On the other hand (the EICA-refined hypothesis [4]), one can assume that invaders will encounter new pathogens in newly established areas, and will allocate energy toward cost-effective immune pathways to permit allocating a non-negligible amount of energy toward other functions. Finally, a last hypothesis (the “immune protection” hypothesis) assumes major changes in pathogen composition between native and invaded areas, which should lead to an overall increase in immune investment by the native species to successfully invade novel environments [4]. This last hypothesis suggests that only non-native species being able to take up the associated costs of immunity will be successful invaders.
The role of immunity in invasion success has yet been poorly investigated, mainly because of the difficulty to simultaneously analyse multiple immune pathways [4]. Charbonnel and collaborators [2] overpass this difficulty by screening all genes expressed (using a whole RNA sequencing approach) in an immune tissue: the spleen. They do so along the invasion routes of two sympatric invasive rodents in Africa and compare anciently and newly invaded areas (respectively). For one of the two species (the house mouse), they found a high number of immune-related genes to be up-regulated in newly invaded areas compared to anciently invaded areas. All categories of immune pathways (costly and cost-effective) were up-regulated, suggesting an overall increase in immune investment in the mouse, which corroborates the “immune protection” hypothesis. For the black rat, patterns of gene expression were somewhat different, with much less pronounced differentiation in gene expression between newly and anciently invaded areas. Among the few differentiated genes, a few were associated to immune responses and some of theses genes were even down-regulated in the newly invaded areas. This pattern may actually corroborate the EICA hypothesis, although it could alternatively suggest that stochastic processes (drift) associated to recent decrease in population size (which is expected during a colonisation event) are more important than selection imposed by pathogens in shaping patterns of immune gene expression.
Overall, this study [2] suggests (i) that immune-related traits are important in predicting invasion success and (ii) that two successful species with a similar invasion history and living in similar environments can use different life-history strategies to reach the same success. This later finding is particularly relevant and intriguing as it suggests that the traits and strategies deployed by species to colonise new habitats might actually be idiosyncratic, and that, if general trends actually emerge in regards of traits predicting the success of invaders, the devil might actually be into the details. Comparative studies are extremely important to identify the general rules and the specificities sustaining actual patterns, but these approaches are yet poorly used in biological invasions (at least empirically). The work presented by Charbonnel and colleagues [2] calls for future comparative studies performed at multiple spatial scales (native vs. non-native areas, anciently vs. recently invaded areas), multiple taxonomic resolutions and across multiple traits (to search for trade-offs), so that the success of invasive species can be properly understood and predicted.
References
[1] Jeschke, J. M., & Strayer, D. L. (2006). Determinants of vertebrate invasion success in Europe and North America. Global Change Biology, 12(9), 1608-1619. doi: 10.1111/j.1365-2486.2006.01213.x
[2] Blossey, B., & Notzold, R. (1995). Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. Journal of Ecology, 83(5), 887-889. doi: 10.2307/2261425
[3] Charbonnel, N., Galan, M., Tatard, C., Loiseau, A., Diagne, C. A., Dalecky, A., Parrinello, H., Rialle, S., Severac, D., & Brouat, C. (2019). Differential immune gene expression associated with contemporary range expansion of two invasive rodents in Senegal. bioRxiv, 442160, ver. 5 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/442160
[4] Lee, K. A., & Klasing, K. C. (2004). A role for immunology in invasion biology. Trends in Ecology & Evolution, 19(10), 523-529. doi: 10.1016/j.tree.2004.07.012
| Differential immune gene expression associated with contemporary range expansion of two invasive rodents in Senegal | Nathalie Charbonnel, Maxime Galan, Caroline Tatard, Anne Loiseau, Christophe Diagne, Ambroise Dalecky, Hugues Parrinello, Stephanie Rialle, Dany Severac and Carine Brouat | <p>Background: Biological invasions are major anthropogenic changes associated with threats to biodiversity and health. What determines the successful establishment of introduced populations still remains unsolved. Here we explore the appealing as... |  | Biological invasions, Eco-immunology & Immunity, Population ecology | Simon Blanchet | | 2018-10-14 12:21:52 | View |
Do the more flexible individuals rely more on causal cognition? Observation versus intervention in causal inference in great-tailed grackles
Aaron Blaisdell, Zoe Johnson-Ulrich, Luisa Bergeron, Carolyn Rowney, Benjamin Seitz, Kelsey McCune, Corina Logan
http://corinalogan.com/Preregistrations/g_causal.html
From cognition to range dynamics: advancing our understanding of macroecological patterns
Recommended by Emanuel A. Fronhofer based on reviews by 2 anonymous reviewers
Understanding the distribution of species on earth is one of the fundamental challenges in ecology and evolution. For a long time, this challenge has mainly been addressed from a correlative point of view with a focus on abiotic factors determining a species abiotic niche (classical bioenvelope models; [1]). It is only recently that researchers have realized that behaviour and especially plasticity in behaviour may play a central role in determining species ranges and their dynamics [e.g., 2-5]. Blaisdell et al. propose to take this even one step further and to analyse how behavioural flexibility and possibly associated causal cognition impacts range dynamics.
The current preregistration is integrated in an ambitious long-term research plan that aims at addressing the above outlined question and focuses specifically on investigating whether more behaviourally flexible individuals are better at deriving causal inferences. The model system the authors plan on using are Great-tailed Grackles which have expanded their range into North America during the last century. The preregistration by Blaisdell et al. is a great example of the future of scientific research: it includes conceptual models, alternative hypotheses and testable predictions along with a sound sampling and analysis plan and embraces the principles of Open Science.
Overall, the research the authors propose is fascinating and of highest relevance, as it aims at bridging scales from the microscopic mechanisms that underlie animal behaviour to macroscopic, macroecological consequences (see also [3]). I am very much looking forward to the results the authors will report.
References
[1] Elith, J. & Leathwick, J. R. 2009. Species distribution models: ecological explanation and prediction across space and time. Annu. Rev. Ecol. Evol. Syst. 40: 677-697. doi: 10.1146/annurev.ecolsys.110308.120159
[2] Kubisch, A.; Degen, T.; Hovestadt, T. & Poethke, H. J. (2013) Predicting range shifts under global change: the balance between local adaptation and dispersal. Ecography 36: 873-882. doi: 10.1111/j.1600-0587.2012.00062.x
[3] Keith, S. A. & Bull, J. W. (2017) Animal culture impacts species' capacity to realise climate-driven range shifts. Ecography, 40: 296-304. doi: 10.1111/ecog.02481
[4] Sullivan, L. L.; Li, B.; Miller, T. E.; Neubert, M. G. & Shaw, A. K. (2017) Density dependence in demography and dispersal generates fluctuating invasion speeds. Proc. Natl. Acad. Sci. USA, 114: 5053-5058. doi: 10.1073/pnas.1618744114
[5] Fronhofer, E. A.; Nitsche, N. & Altermatt, F. (2017) Information use shapes the dynamics of range expansions into environmental gradients. Glob. Ecol. Biogeogr. 26: 400-411. doi: 10.1111/geb.12547
| Do the more flexible individuals rely more on causal cognition? Observation versus intervention in causal inference in great-tailed grackles | Aaron Blaisdell, Zoe Johnson-Ulrich, Luisa Bergeron, Carolyn Rowney, Benjamin Seitz, Kelsey McCune, Corina Logan | This PREREGISTRATION has undergone one round of peer reviews. We have now revised the preregistration and addressed reviewer comments. The DOI was issued by OSF and refers to the whole GitHub repository, which contains multiple files. The specific... |  | Behaviour & Ethology, Preregistrations, Zoology | Emanuel A. Fronhofer | | 2018-08-20 11:09:48 | View |
Inferring macro-ecological patterns from local species' occurrences
Anna Tovo, Marco Formentin, Samir Suweis, Samuele Stivanello, Sandro Azaele, Amos Maritan
https://doi.org/10.1101/387456
Upscaling the neighborhood: how to get species diversity, abundance and range distributions from local presence/absence data
Recommended by Matthieu Barbier based on reviews by Kevin Cazelles and 1 anonymous reviewer
How do you estimate the biodiversity of a whole community, or the distribution of abundances and ranges of its species, from presence/absence data in scattered samples?
It all starts with the collector's dilemma: if you double the number of samples, you will not get double the number of species, since you will find many of the same common species, and only a few new rare ones.
This non-additivity has prompted many ecologists to study the Species-Area Relationship. A common theoretical approach has been to connect this spatial pattern to the overall distribution of how common or rare a species can be. At least since Fisher's celebrated log-series [1], ecologists have been trying to, first, infer the shape of the Species Abundance Distribution, and then, use it to predict how many species should be found in a given area or a given number of samples. This has found many applications, from microbial communities to tropical forests, from estimating the number of yet-unknown species to predicting how much biodiversity may be lost if a fraction of the habitat is removed.
In this elegant work, Tovo et al. [2] propose a method that starts only from presence/absence data over a number of samples, and provides the community's diversity, as well as its abundance and range size distributions. This method is simple, analytically explicit, and accurate: the authors test it on the classic Pasoh and Barro Colorado Island tropical forest datasets, and on simulated data. They make a very laudable effort in both explaining its theoretical underpinnings, and proposing a straightforward step-by-step guide to applying it to data.
The core of Tovo et al's method is a simple property: the scale invariance of the Negative Binomial (NB) distribution. Subsampling from a NB gives another NB, where a single parameter has changed. Therefore, if the Species Abundance Distribution is close enough to some NB (which is flexible enough to accommodate all the data here), we can estimate how this parameter changes when going from (1) a single sample to (2) all the available samples, and from there, extrapolate to (3) the entire community.
This principle was first applied by the authors in a previous study [3] that required abundance data in the samples, rather than just presence/absence. Given that binary occurrence data is far more available in a variety of empirical settings, this extension is worthwhile (including its new predictions on range size distributions), and it deserves to be widely known and tested.
ADDITIONAL COMMENTS
1) To explain the novelty of the authors' contribution, it is useful to look at competing techniques.
Some ""parametric"" approaches try to infer the whole-community Species Abundance Distribution (SAD) by guessing its functional form (Gaussian, power-law, log-series...) and fitting its parameters from sampled data. The issue is that this distribution shape may not remain in the same family as we increase the sampling effort or area, so the regression problem may not be well-defined. This is where the Negative Binomial's scale invariance is useful.
Other ""non-parametric"" approaches have renounced guessing the whole SAD: they simply try to approximate of its tail of rare species, by looking at how many species are found in only one (or a few) samples. From this, they derive an estimate of biodiversity that is agnostic to the rest of the SAD. Tovo et al. [2] show the issue with these approaches: they extrapolate from the properties of individual samples to the whole community, but do not properly account for the bias introduced by the amount of sampling (the intermediate scale (2) in the summary above).
2) The main condition for all such approaches to work is well-mixedness: each sample should be sufficiently like a lot drawn from the same skewed lottery. As long as that condition applies, finding the best approach is a theoretical matter of probabilities and combinatorics that may, in time, be given a definite answer.
The authors also show that ""well-mixed"" is not as restrictive as it sounds: the method works both on real data (which is never perfectly mixed) and on simulations where species are even more spatially clustered than the empirical data. In addition, the Negative Binomial's scale invariance entails that, if it works well enough at some spatial scale, it will also work at all higher scales (until one reaches the edges of the sufficiently-well-mixed community)
3) One may ask: why the Negative Binomial as a Species Abundance Distribution?
If one wishes for some dynamical explanation, the Negative Binomial can be derived from neutral birth and death process with immigration, as shown by the authors in [3]. But to be applied to data, it should only be able to approximate the empirical distribution well enough (at all relevant scales). Depending on one's taste, this type of probabilistic approaches can be interpreted as:
- purely phenomenological, describing only the observational process of sampling from an existing state of affairs, not the ecological processes that gave rise to that state.
- a null model, from which everything in practice is expected to deviate to some extent.
- or a way to capture the statistical forces that tend to induce stable relationships between different patterns (as long as no ecological process opposes them strongly enough).
References
[1] Fisher, R. A., Corbet, A. S., & Williams, C. B. (1943). The relation between the number of species and the number of individuals in a random sample of an animal population. The Journal of Animal Ecology, 42-58. doi: 10.2307/1411
[2] Tovo, A., Formentin, M., Suweis, S., Stivanello, S., Azaele, S., & Maritan, A. (2019). Inferring macro-ecological patterns from local species' occurrences. bioRxiv, 387456, ver. 2 peer-reviewed and recommended by PCI Ecol. doi: 10.1101/387456
[3] Tovo, A., Suweis, S., Formentin, M., Favretti, M., Volkov, I., Banavar, J. R., Azaele, S., & Maritan, A. (2017). Upscaling species richness and abundances in tropical forests. Science Advances, 3(10), e1701438. doi: 10.1126/sciadv.1701438
| Inferring macro-ecological patterns from local species' occurrences | Anna Tovo, Marco Formentin, Samir Suweis, Samuele Stivanello, Sandro Azaele, Amos Maritan | <p>Biodiversity provides support for life, vital provisions, regulating services and has positive cultural impacts. It is therefore important to have accurate methods to measure biodiversity, in order to safeguard it when we discover it to be thre... |  | Macroecology, Species distributions, Statistical ecology, Theoretical ecology | Matthieu Barbier | | 2018-08-09 16:44:09 | View |
