The introduction of Ludwigia species as ornamental plants in both North America and Europe dates back almost two centuries, during which time they expanded as naturalized and later invasive species in these territories (Dandelot et al. 2005, Okada et al. 2009). Repeated deliberate or non-deliberate introductions over time of this species complex that can hybridize has given rise to an evolutionarily complex scenario, which is compounded by the difficulty in delimiting some of these species and by the diversity of their modes of reproduction.

Dandelot (2004) and Dandelot et al. (2005) determined the presence of two Ludwigia taxa in France, L. peploides subsp. montevidensis (Spreng.) P.H.Raven (here after Lpm), and L. grandiflora subsp. hexapetala (Hook. & Arn.) G.L.Nesom & Kartesz (here after Lgh), based on their cytotypes (2n = 16, and 2n = 80, respectively) and without evidence of hybridization between them. Furthermore, despite a predominantly vegetative reproduction observed for both species, they differed in their breeding systems. While Lpm is self-compatible and produce a high number of viable seeds in all populations, Lgh is self-incompatible and its populations may drastically differ in seed viability (Dandelot 2004). Several years later, Portillo-Lemus et al. (2021) determined that the differences in seed production between some populations of Lgh are due to the existence of a heteromorphic reproductive system in this taxon, involving a self-incompatible morph (long-style morph; hereafter L-morph), and a self-compatible morph (short-style morph: hereafter S-morph). Moreover, Portillo-Lemus et al. (2022) observed that self-pollen in the L-morph flowers stop growing lately (i.e., in the ovarian area) without fertilizing the ovules, concluding that a late-acting self-incompatible system (hereafter, LSI) is present in this morph.

At this point, it is relevant to understand the possible interactions between populations of different morphs in Lgh, and the implications that they may have on their expansive success in non-native areas in order to develop more effective management plans. To achieve this goal, Stoeckel et al. (2024) analyzed the population genetics in 53 Lgh populations in western Europe (without finding any Lpm population in the sampling area), 40 of which exclusively presented the L-morph and 13 the S-morph. This fact offered the opportunity to compare and interpret the differences between populations of different morphs in Lgh. Other previous works on genetic diversity of Lgh in peripatric or non-native areas pointed to a high clonality and an extremely low genetic diversity (Okada et al. 2009, Armitage et al. 2013), concluding in a monoclonal or few ancestral original clones for these invasive populations.

However, the investigations of Stoeckel et al. (2024) found a high genetic diversity in all populations of Lgh studied despite their predominant clonal reproduction. Interestingly, they found that sexual reproduction is also present, not only in the S-morph by selfing, but also in the L-morph, although limited and preferably by allogamy. They discuss the advantages and drawbacks of the different modes of reproduction observed in Lgh populations, the interactions among them, and the implications that both, the scarcely documented LSI (Gibbs 2014) and selfing, have in the reproductive success and in the maintenance of the high genetic diversity observed in Lgh in western Europe.

The contrasting results with the previous ones (Okada et al. 2009, Armitage et al. 2013) stress the relevance of using appropriate markers and analyses to assess the genetic diversity in autoployploid species, as well as the necessity of knowing the modes of reproduction in the populations studied for an optimal interpretation of the genetic metrics. The approach of the study by Stoeckel et al. (2024) had the challenge of having found suitable markers to deal with a taxon of complex origin such as Lgh, whose genome is compound by a set of autotetraploid chromosomes shared with Lpm and traces of ancient hybridizations of other diploid lineages (Barloy et al. 2024). Using RAD-Seq, Stoeckel et al. (2024) generated an original set of 36 polymorphic SNPs shared between Lgh and Lpm ensuring that these SNPs belong to the tetraploid part of the Lgh genome derived from Lpm. Another interesting contribution of this work is the exhaustive analysis of several genetic descriptors (indexes) and the interpretative guide they provide for each of them in relation to the different modes of reproduction of the study system. Finally, they propose a pair of very useful synthetic indices (i.e., clonality index and selfing index), since they allow to classify populations according to their levels of clonality and selfing.

Stoeckel et al. (2024) conclude the relevance that selfing and LSI populations, and the hybridization between them may have on the expansion and success of invasive plant species, and the necessity to know the modes of reproduction of these populations jointly with their genetic diversity in order to develop appropriate management plans. This study raises new questions such as the modes of reproduction and genetic diversity and structure have other Lgh populations, both invasive and native, and the dynamics of these populations under different future scenarios.

References

Armitage, J. D., Könyves, K., Bailey, J. P., David, J. C., & Culham, A. (2013). A molecular, morphological and cytological investigation of the identity of non-native Ludwigia (Onagraceae) populations in Britain. New Journal of Botany, 3(2), 88–95. https://doi.org/10.1179/2042349713Y.0000000023

Barloy, D., Lemus, L. P.-, Krueger-Hadfield, S. A., Huteau, V., & Coriton, O. (2024). Genomic relationships among diploid and polyploid species of the genus Ludwigia L. section Jussiaea using a combination of cytogenetic, morphological, and crossing investigations. ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2023.01.02.522458

Dandelot, S. (2004). Les Ludwigia spp. invasives du Sud de la France: Historique, Biosystématique, Biologie et Ecologie [PhD thesis, Aix-Marseille 3]. https://www.theses.fr/2004AIX30052

Dandelot, S., Verlaque, R., Dutartre, A., & Cazaubon, A. (2005). Ecological, dynamic and taxonomic problems due to Ludwigia (Onagraceae) in France. Hydrobiologia, 551(1), 131–136. https://doi.org/10.1007/s10750-005-4455-0

Gibbs, P. E. (2014). Late-acting self-incompatibility – the pariah breeding system in flowering plants. New Phytologist, 203(3), 717–734. https://doi.org/10.1111/nph.12874

Okada, M., Grewell, B. J., & Jasieniuk, M. (2009). Clonal spread of invasive Ludwigia hexapetala and L. grandiflora in freshwater wetlands of California. Aquatic Botany, 91(3), 123–129. https://doi.org/10.1016/j.aquabot.2009.03.006

Portillo Lemus, L. O., Bozec, M., Harang, M., Coudreuse, J., Haury, J., Stoeckel, S., & Barloy, D. (2021). Self-incompatibility limits sexual reproduction rather than environmental conditions in an invasive water primrose. Plant-Environment Interactions, 2(2), 74–86. https://doi.org/10.1002/pei3.10042

Portillo Lemus, L. O., Harang, M., Bozec, M., Haury, J., Stoeckel, S., & Barloy, D. (2022). Late-acting self-incompatible system, preferential allogamy and delayed selfing in the heteromorphic invasive populations of Ludwigia grandiflora subsp. hexapetala. Peer Community Journal, 2. https://doi.org/10.24072/pcjournal.108

Stoeckel, S., Becheler, R., Portillo-Lemus, L., Harang, M., Besnard, A.-L., Lassalle, G., Causse-Védrines, R., Michon-Coudouel, S., Park D. J., Pope, B. J., Petit, E. J. & Barloy, D. (2024) Reproductive modes in populations of late-acting self-incompatible and self-compatible polyploid Ludwigia grandiflora subsp. hexapetala in western Europe. biorxiv, ver.4 peer-reviewed and recommended by PCI Evol Biol https://doi.org/10.1101/2024.03.21.586104

Foraging has been long been studied from an economic perspective, where the costs and benefits of foraging decisions are measured in terms of a single currency of energy which is then taken as a proxy for fitness. A mainstay foraging theory is Charnov’s Marginal Value Theorem (Charnov, 1976), or MVT, which includes a graphical interpretation and has been applied to an enormous range topics in behavioral ecology (Menezes , 2022). Empirical studies often find that animals deviate from MVT, sometimes in that they predictably stay longer than the optimal time. One explanation for this comes from state based models of behavior (Nonacs 2001)

Now Calcgano and colleagues (2024) set out to extend and unify foraging models that include various aspects of risk to the foragers, and propose using a  risk MVT, or rMVT. They consider three types of risk that foragers face, disturbance, escape, and death. Disturbance represents scenarios where the forager is either physically interrupted in their foraging, or stops foraging temporarily because of the presence of a predator (i.e. a fear response). Such a disturbance can be thought of as altering the gain function for resources acquired while foraging in the patch, allowing the rMVT to be applied in a familiar way with only a reinterpretation of the gain function.  In the escape scenarios, foragers are forced to leave a patch because of predator behavior, and therefore artificially decrease their foraging time as compared with their desired foraging time. Now, optimization can be calculated based on this expected time foraging, which means that in effect the forager compensates for the reduced time in the patch by modifying their view of how long they will actually forage.

Finally they consider scenarios where risk may result in death, and further divide this into two cases, one where foraging returns are instantaneously converted to fitness, and another where they are only converted in between foraging bouts. This represents an important case to consider, because the total number of foraging trips now depends on the rate of predator attack. In these scenarios, the boldness of the forager is decreased and they become more risk-averse.

The authors find that under the disturbance and escape scenarios, patch residence time can actually go up with risk. This is in effect because they are depleting the patch less per unit time, because a larger fraction of time is taken up with avoiding predators. In terms of field applications, this may differ from what is typically considered as risk, since harassment by conspecifics has the same disturbance effect as predator avoidance behaviors.

Most experiments on foraging are done in the absence of risk or signals of risk, i.e. in laboratory or otherwise controlled environments. The rMVT predictions deviate from non-risk scenarios in complex ways, in that the patch residence time may increase or decrease under risk. It is also important to note that foragers have evolved their foraging strategies in response to the risk profiles that they have historically experienced, and therefore experiments lacking risk may still show that foragers alter their behavior from the MVT predictions in a way that reflects historical levels of risk.

References

Calcagno, V.,  Grognard, F., Hamelin, F.M. and  Mailleret, L. (2024). Taking fear back into the Marginal Value Theorem: the risk-MVT and optimal boldness. bioRxiv, 2023.10.31.564970, ver. 3 peer-reviewed and recommended by PCI Evolutionary Biology.  https://doi.org/10.1101/2023.10.31.564970

Charnov E. (1976). Optimal foraging the marginal value theorem. Theor Popul Biol. 9, 129–136.

Menezes, JFS (2022).The marginal value theorem as a special case of the ideal free distribution. Ecological Modelling 468:109933. https://doi.org/10.1016/j.ecolmodel.2022.109933

Nonacs, P. 2001.  State dependent behavior and the Marginal Value Theorem. Behavioral Ecology 12(1) 71–83. https://doi.org/10.1093/oxfordjournals.beheco.a000381

At the very end of a paper entitled "Copepodology for the ornithologist" Hutchinson (1951) pointed out the possibility of 'fugitive species'.  A fugitive species, said Hutchinson, is one that we would typically think of as competitively inferior.  Wherever it happens to live it will eventually be overwhelmed by competition from another species.  We would expect it to rapidly go extinct but for one reason: it happens to be a much better coloniser than the other species.  Now all we need to explain its persistence is a dose of space and a little disturbance: a world in which there are occasional disturbances that cause local extinction of the dominant species. Now, argued Hutchinson, we have a recipe for persistence, albeit of a harried kind.  As Hutchinson put it, fugitive species "are forever on the move, always becoming extinct in one locality as they succumb to competition, and always surviving as they reestablish themselves in some other locality."

It is a fascinating idea, not just because it points to an interesting strategy, but also because it enriches our idea of competition: competition for space can be just as important as competition for time.

Hutchinson's idea was independently discovered with the advent of metapopulation theory (Levins 1971; Slatkin 1974) and since then, of course, ecologists have gone looking, and they have unearthed many examples of species that could be said to have a fugitive lifestyle.  These fugitive species are out there, but we don't often get to see them evolve.  

In their recent paper, Chapuis et al. (2024) make a convincing case that they have seen the evolution of a fugitive species.  They catalog the arrival of an invasive freshwater snail on Guadeloupe in the Lesser Antilles, and they wonder what impact this snail's arrival might have on a native freshwater snail.  This is a snail invasion, so it has been proceeding at a majestic pace, allowing the researchers to compare populations of the native snail that are completely naive to the invader with those that have been exposed to the invader for either a relatively short period (<20 generations) or longer periods (>20 generations).  They undertook an extensive set of competition assays on these snails to find out which species were competitively superior and how the native species' competitive ability has evolved over time.

Against naive populations of the native, the invasive snail turns out to be unequivocally the stronger competitor.  (This makes sense; it probably wouldn't have been able to invade if it wasn't.)  So what about populations of the native snail that have been exposed for longer, that have had time to adapt?  Surprisingly these populations appear to have evolved to become even weaker competitors than they already were. 

So why is it that the native species has not simply been driven extinct? Drawing on their previous work on this system, the authors can explain this situation.  The native species appears to be the better coloniser of new habitats.  Thus, it appears that the arrival of the invasive species has pushed the native species into a different place along the competition-colonisation axis.  It has sacrificed competitive ability in favour of becoming a better coloniser; it has become a fugitive species in its own backyard.

This is a really nice empirical study.  It is a large lab study, but one that makes careful sampling around a dynamic field situation.  Thus, it is a lab study that informs an earlier body of fieldwork and so reveals a fascinating story about what is happening in the field. We are left not only with a particularly compelling example of character displacement towards a colonising phenotype but also with something a little less scientific: the image of a hobo snail, forever on the run, surviving in the spaces in between.

References

Chapuis E, Jarne P, David P (2024) Rapid life-history evolution reinforces competitive asymmetry between invasive and resident species. bioRxiv, 2023.10.25.563987, ver. 2 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2023.10.25.563987

Hutchinson, G.E. (1951) Copepodology for the Ornithologist. Ecology 32: 571–77. https://doi.org/10.2307/1931746

Levins, R., and D. Culver. (1971) Regional Coexistence of Species and Competition between Rare Species. Proceedings of the National Academy of Sciences 68, no. 6: 1246–48. https://doi.org/10.1073/pnas.68.6.1246.

Slatkin, Montgomery. (1974) Competition and Regional Coexistence. Ecology 55, no. 1: 128–34. https://doi.org/10.2307/1934625.

Understanding how populations evolve under thermal stress and how this process shapes the response of other stress responses is an important research topic in the context of thermal adaptation and climate change. In a thermal experimental evolution study in Drosophila subobscura, Castañeda (2024) addressed the correlated responses to selection for increasing knockdown temperature in different resistance traits, either directly related to thermal stress (e.g. knockdown time at different temperatures and CTmax) or not (e.g. desiccation and starvation resistance). 

The author found that the evolution of higher knockdown temperature did in fact lead to correlated responses in other stress traits. While such correlations might be expected for the thermal stress traits measured (knockdown time and CTmax), it was perhaps less expectable for desiccation and starvation resistance. However, the general occurrence of correlated evolutionary responses between stressors has been previously described, namely in Drosophila (e.g. see Bubliy and Loeschcke 2005), pointing to a possible genetic link between distinct (thermal) stress traits. 

There are however some features that make the findings of this study rather appealing. First, the evidence that the correlated stress responses depend on the intensity of thermal selection (i.e. the warming rate) and on the sex of the organisms. Second, correlated patterns of both desiccation and starvation resistance highlight the possibility of the evolution of a cross-tolerance response, which might positively impact on population ability to evolve under sustained stressful environments (Rodgers and Gomez Izasa 2023). However, it is important to point out that the correlated patterns between these two resistance traits (desiccation and starvation) were not exactly consistent. In fact, the negative correlated response observed for female starvation resistance is thought provoking and argues again a general scenario of cross-tolerance. 

While these findings are a step forward for a more multifaceted understanding of thermal adaptation in the context of stressful environments, they also highlight the need for further studies of thermal adaptation namely 1) addressing the underlying physiological and genomic mechanisms that link male and female heat tolerance and the response to other stress resistance traits (namely starvation resistance); 2) testing the extent to which cross-resistance patterns can be generalized to different thermal selection contexts and populations. 

In addition, this study also opens new questions considering the scope of correlated evolution to other stress traits, that might be relevant in diverse ecological scenarios. For instance, does selection towards higher heat resistance lead to correlated evolution of cold resistance? And under which circumstances (e.g. different heat selection intensities)?  In fact, the occurrence of a positive (or negative) correlation cold and heat stress responses is a topic of high interest, with relevant ecological implications particularly considering the increased thermal fluctuations in natural environments because of climate warming. Cross-tolerance between cold and heat stress responses has been described (Singh 2022, Rodgers and Gomez Izasa 2023). On the other hand, negative correlations (i.e. trade-offs) between these stress traits (Stazione et al. 2020; Schou et al 2022) can impact negatively on populations’ ability to withstand thermal variability. 

As climatic changes proceed leading to increasing environmental variability, empirical studies such as that of Castañeda (2024) are critical in the pursue for a multivariate perspective on trait evolution in scenarios of climate change adaptation. Understanding how tolerance to different environmental stressors may evolve and which factors can act as drivers of that variation will ultimately enable better forecasts of climate change effects on biodiversity in nature.

References

Castañeda, LE. Cross-tolerance evolution is driven by selection on heat tolerance in Drosophila subobscura. Biorxiv, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology (2024). https://www.doi.org/10.1101/2023.09.05.556367

Bubliy, OA, Loeschcke, V. Correlated responses to selection for stress resistance and longevity in a laboratory population of Drosophila melanogaster. J Evol Biol. 18(4):789-803 (2005). https://www.doi.org/10.1111/j.1420-9101.2005.00928.x. 

Rodgers, EM, Gomez Isaza, DF. The mechanistic basis and adaptive significance of cross-tolerance: a 'pre-adaptation' to a changing world? J Exp Biol. 226(11):jeb245644 (2023). https://www.doi.org/10.1242/jeb.245644. 

Schou, MF, Engelbrecht, A, Brand, Z, Svensson, EI, Cloete, S, Cornwallis, CK. Evolutionary trade-offs between heat and cold tolerance limit responses to fluctuating climates. Sci Adv. 8(21):eabn9580 (2022). https://www.doi.org/10.1126/sciadv.abn9580. 

Singh, K, Arun Samant, M, Prasad, NG. Evolution of cross-tolerance in Drosophila melanogaster as a result of increased resistance to cold stress. Sci Rep. 12(1):19536 (2022). https://www.doi.org/10.1038/s41598-022-23674-z.

Stazione, L, Norry, FM, Gomez, FH, Sambucetti, P. Heat knockdown resistance and chill-coma recovery as correlated responses to selection on mating success at high temperature in Drosophila buzzatii. Ecol Evol. 10(4):1998-2006 (2020). https://www.doi.org/10.1002/ece3.6032.

Although most mutations are deleterious, the strongly deleterious ones do not spread in a very large population as their chance of fixation is very small. Another mechanism via which the deleterious mutations can be eliminated is via recombination or sexual reproduction. However, in a finite asexual population, the subpopulation without any deleterious mutation will eventually acquire a deleterious mutation resulting in the reduction of the population size or in other words, an increase in the genetic drift. This, in turn, will lead the population to acquire deleterious mutations at a faster rate eventually leading to a mutational meltdown.

This irreversible (or, at least over some long time scales) accumulation of deleterious mutations is especially relevant to RNA viruses due to their high mutation rate, and while the prior work has dealt with bacteriophages and RNA viruses, the study by Lafforgue et al. [1] makes an interesting contribution to the existing literature by focusing on plants.

In this study, the authors enquire how despite the repeated increase in the strength of genetic drift, how the RNA viruses manage to survive in plants. Following a series of experiments and some numerical simulations, the authors find that as expected, after severe bottlenecks, the fitness of the population decreases significantly. But if the bottlenecks are followed by population expansion, the Muller’s ratchet can be halted due to the genetic diversity generated during population growth. They hypothesize this mechanism as a potential way by which the RNA viruses can survive the mutational meltdown.

As a theoretician, I find this investigation quite interesting and would like to see more studies addressing, e.g., the minimum population growth rate required to counter the potential extinction for a given bottleneck size and deleterious mutation rate. Of course, it would be interesting to see in future work if the hypothesis in this article can be tested in natural populations.

References

[1] Guillaume Lafforgue, Marie Lefebvre, Thierry Michon, Santiago F. Elena (2024) How do plant RNA viruses overcome the negative effect of Muller s ratchet despite strong transmission bottlenecks? bioRxiv, ver. 3 peer-reviewed and recommended by Peer Community In Evolutionary Biology
https://doi.org/10.1101/2023.08.01.550272