The evolutionary response of populations to changing or novel environments is a topic that unites the interests of evolutionary biologists, ecologists, and biomedical researchers [1]. A prominent phenomenon in this research area is evolutionary rescue, whereby a population that is otherwise doomed to extinction survives due to the spread of new or pre-existing mutations that are beneficial in the new environment. Scenarios of evolutionary rescue require a specific set of parameters: the absolute growth rate has to be negative before the rescue mechanism spreads, upon which the growth rate becomes positive. However, potential examples of its relevance exist (e.g., [2]). From a theoretical point of view, the technical challenge but also the beauty of evolutionary rescue models is that they combine the study of population dynamics (i.e., changes in the size of populations) and population genetics (i.e., changes in the frequencies in the population). Together, the potential relevance of evolutionary rescue in nature and the models' theoretical appeal has resulted in a suite of modeling studies on the subject in recent years.
In this manuscript [3], Tomasini and Peischl address a question that has been contentiously discussed in the literature: when does migration favor evolutionary rescue? They expand on past work (specifically, [4, 5]) by studying the influence of the interaction of the speed and severity of environmental change and the amount of dispersal on the probability of evolutionary rescue. They develop simple analytical results (complemented by simulations) for a haploid one-locus model of two populations connected by gene flow, where both populations deteriorate successively such that evolutionary rescue is required for the metapopulation to survive. For example, the authors derive a simple analytical condition demonstrating that migration between the subpopulations favors evolutionary rescue if environmental change occurs slowly across the two populations (which leaves time for the second population to serve as an immigration source), if the new environment is very harsh and/or if rescue mutations are strongly beneficial in the new environment. The latter conditions ensure that the rescue mutations can spread easily in the new environment without much competition with immigrating, maladapted, genotypes. This result is intuitive and connects between traditional single and multiple-deme models.
Altogether, Tomasini and Peischl present an extensive theoretical study and address also the effect of various tweaks to the model assumptions, such as asymmetries in gene flow and/or carrying capacities, and the effects of different density regulation and local growth rates. They successfully made an effort to explain and interpret their results for a general audience, such that also non-theoreticians should not be afraid to take a look at this manuscript.

References

[1] Bell, G. (2017). Evolutionary Rescue. Annual Review of Ecology, Evolution, and Systematics 48(1), 605-627. doi: 10.1146/annurev-ecolsys-110316-023011
[2] Oziolor, E. M., Reid, N. M., Yair, S. et al. (2019). Adaptive introgression enables evolutionary rescue from extreme environmental pollution. Science, 364(6439), 455-457. doi: 10.1126/science.aav4155
[3] Tomasini, M. and Peischl, S. (2020) When does gene flow facilitate evolutionary rescue? bioRxiv, 622142, ver. 5 peer-reviewed and recommended by PCI Evolutionary Biology. doi: 10.1101/622142
[4] Uecker, H., Otto, S. P., and Hermisson, J. (2014). Evolutionary rescue in structured populations. The American Naturalist, 183(1), E17-E35. doi: 10.1086/673914
[5] Tomasini, M., and Peischl, S. (2018). Establishment of locally adapted mutations under divergent selection. Genetics, 209(3), 885-895. doi: 10.1534/genetics.118.301104

Within-host parasite density is tightly linked to parasite fitness often determining both transmission success and virulence (parasite-induced harm to the host) (Alizon et al., 2009, Anderson & May, 1982). Parasite density may thus be controlled by selection balancing these conflicting pressures. Actual within-host density regulation may be under host or parasite control, or due to other environmental factors (Wale et al., 2019, Vale et al., 2011, Chrostek et al., 2013). Vertically transmitted parasites may also be more vulnerable to drift associated with bottlenecks between generations, which may also determine within-host population size (Mathe-Hubert et al., 2019, Mira & Moran, 2002).

Bénard et al. (2021) use 3 experiments to disentangle the role of drift versus host factors in the control of within-host Wolbachia growth in Drosophila melanogaster. They use the wMelPop Wolbachia strain in which virulence (fly longevity) and within-host growth correlate positively with copy number in the genomic region Octomom (Chrostek et al., 2013, Chrostek & Teixeira, 2015). Octomom copy number can be used as a marker for different genetic lineages within the wMelPop strain.

In a first experiment, they introgressed and backcrossed this Wolbachia strain into 6 different host genetic backgrounds and show striking differences in within-host symbiont densities which correlate positively with Octomom copy number. This is consistent with host genotype selecting different Wolbachia strains, but also with bottlenecks and drift between generations. To distinguish between these possibilities, they perform 2 further experiments. 

A second experiment repeated experiment 1, but this time introgression was into 3 independent lines of the Bolivia and USA Drosophila populations; those that, respectively, exhibited the lowest and highest Wolbachia density and Octomom copy number. In this experiment, growth and Octomom copy number were measured across the 3 lines, for each population, after 1, 13 and 25 generations. Although there were little differences between replicates at generation 1, there were differences at generations 13 and 25 among the replicates of both the Bolivia and USA lines. These results are indicative of parasite control, or drift being responsible for within-host growth rather than host factors. 

A third experiment tested whether Wolbachia density and copy number were under host or parasite control. This was done, again using the USA and Bolivia lines, but this time those from the first experiment, several generations following the initial introgression and backcrossing. The newly introgressed lines were again followed for 25 generations. At generation 1, Wolbachia phenotypes resembled those of the donor parasite population and not the recipient host population indicating a possible maternal effect, but a lack of host control over the parasite. Furthermore, Wolbachia densities and Octomom number differed among replicate lines through time for Bolivia populations and from the donor parasite lines for both populations. These differences among replicate lines that share both host and parasite origins suggest that drift and/or maternal effects are responsible for within-host Wolbachia density and Octomom number. 

These findings indicate that drift appears to play a role in shaping Wolbachia evolution in this system. Nevertheless, completely ruling out the role of the host or parasite in controlling densities will require further study. The findings of Bénard and coworkers (2021) should stimulate future work on the contribution of drift to the evolution of vertically transmitted parasites.

References

Alizon S, Hurford A, Mideo N, Baalen MV (2009) Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. Journal of Evolutionary Biology, 22, 245–259. https://doi.org/10.1111/j.1420-9101.2008.01658.x

Anderson RM, May RM (1982) Coevolution of hosts and parasites. Parasitology, 85, 411–426. https://doi.org/10.1017/S0031182000055360

Bénard A, Henri H, Noûs C, Vavre F, Kremer N (2021) Wolbachia load variation in Drosophila is more likely caused by drift than by host genetic factors. bioRxiv, 2020.11.29.402545, ver. 4  recommended and peer-reviewed by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2020.11.29.402545

Chrostek E, Marialva MSP, Esteves SS, Weinert LA, Martinez J, Jiggins FM, Teixeira L (2013) Wolbachia Variants Induce Differential Protection to Viruses in Drosophila melanogaster: A Phenotypic and Phylogenomic Analysis. PLOS Genetics, 9, e1003896. https://doi.org/10.1371/journal.pgen.1003896

Chrostek E, Teixeira L (2015) Mutualism Breakdown by Amplification of Wolbachia Genes. PLOS Biology, 13, e1002065. https://doi.org/10.1371/journal.pbio.1002065

Mathé‐Hubert H, Kaech H, Hertaeg C, Jaenike J, Vorburger C (2019) Nonrandom associations of maternally transmitted symbionts in insects: The roles of drift versus biased cotransmission and selection. Molecular Ecology, 28, 5330–5346. https://doi.org/10.1111/mec.15206

Mira A, Moran NA (2002) Estimating Population Size and Transmission Bottlenecks in Maternally Transmitted Endosymbiotic Bacteria. Microbial Ecology, 44, 137–143. https://doi.org/10.1007/s00248-002-0012-9

Vale PF, Wilson AJ, Best A, Boots M, Little TJ (2011) Epidemiological, Evolutionary, and Coevolutionary Implications of Context-Dependent Parasitism. The American Naturalist, 177, 510–521. https://doi.org/10.1086/659002

Wale N, Jones MJ, Sim DG, Read AF, King AA (2019) The contribution of host cell-directed vs. parasite-directed immunity to the disease and dynamics of malaria infections. Proceedings of the National Academy of Sciences, 116, 22386–22392. https://doi.org/10.1073/pnas.1908147116

 

Historically neglected or considered a rare aberration in animals under the biological species concept, interspecific hybridisation has by now been recognised to be taxonomically widespread, particularly in rapidly diversifying groups (Dagilis et al. 2021; Edelman & Mallet 2021; Mallet et al. 2016; Seehausen 2004). Yet the prevalence of introgressive hybridizations, its evolutionary significance, and its impact on species diversification remain a hot topic of research in evolutionary biology. The rapid increase in genomic resources now available for non-model species has significantly contributed to the detection of introgressive hybridization across taxa showing that reticulated evolution is far more common in the animal kingdom than historically considered. Yet, detecting it, quantifying its magnitude, and assessing its evolutionary significance remains a challenging endeavour with constantly evolving methodologies to better explore and exploit genomic data (Blair & Ané 2020; Degnan & Rosenberg 2009; Edelman & Mallet 2021; Hibbins & Hahn 2022).

In the marine realm, the dearth of geographic barriers and the large dispersal abilities of pelagic species like cetaceans have raised the questions of how populations and species can diverge and adapt to distinct ecological conditions in face of potentially large gene-flow, the so-called marine speciation paradox (Bierne et al. 2003). Contemporaneous hybridization among cetacean species has been widely documented in nature despite large phenotypic differences (Crossman et al. 2016). The historical prevalence of reticulated evolution, its evolutionary significance, and how it might have impacted the evolutionary history and diversification of the cetaceans have however remained elusive so far. Recent phylogenomic studies suggested that introgression has been prevalent in cetacean evolutionary history with instances reported among baleen whales (mysticetes) (Árnason et al. 2018) and among toothed whales (odontocetes), especially in the rapidly diversifying dolphins family of the Delphininae (Guo et al. 2021; Moura et al. 2020).

Analysing publicly available whole-genome data from nine cetacean species across three families of Delphinoidae – dolphins, porpoises, and monondontidae – using phylogenomics and demo-genetics approaches, Westbury and colleagues (2022) take a step further in documenting that evolution among these species has been far from a simple bifurcating tree. Instead, their study describes widespread occurrences of introgression among Delphinoidae, drawing a complex picture of reticulated evolutionary history. After describing major topology discordance in phylogenetic gene trees along the genome, the authors use a panel of approaches to disentangle introgression from incomplete lineage sorting (ILS), the two most common causes of tree topology discordances (Hibbins & Hahn 2022). Applying popular tests that separate introgression from ILS, such as the Patterson’s D (a.k.a. ABBA-BABA) test (Durand et al. 2011; Green et al. 2010), QuIBL (Edelman et al. 2019), and D-FOIL (Pease & Hahn 2015), the authors report that signals of introgression are present in the genomes of most (if not all) the cetacean species included in their study. However, this picture needs to be nuanced. Most introgression signals seem to echo old introgression events that occurred primarily among ancestors. This is suggested by the differential signals of topology discordance along the genome when considering sliding windows along the genome of varying sizes (50kb, 100kb, and 1Mb), and by patterns of excess derived allele sharing along branches of the species tree, as captured by the f-branch test (Malinsky et al. 2021; Malinsky et al. 2018). The authors further investigated the dynamic of cessation of gene flow (and/or ILS) between species using the F1 hybrid PSMC (or hPSMC) approach (Cahill et al. 2016). By estimating the cross-coalescent rates (CRR) between species pairs with time in light of previously estimated species divergence times (McGowen et al. 2020), the authors report that gene flow (and/or ILS) most likely has stopped by now among most species, but it may have lasted for more than half of the time since the species split from each other. According to the author, this result may reflect the slow process by which reproductive isolation would have evolved between cetacean lineages, and that species isolation was marked by significant introgression events.

Now, while the present study provides a good overview of how complex is the reticulated evolutionary history of the Delphinoidae, getting a complete picture will require overcoming a few important limitations. The first ones are methodological and related to the phylogenomic analyses. Given the sampling design with one diploid genome per species, the authors could not phase the data into the parental haplotypes, but instead relied on a majority consensus creating mosaic haploidized genomes representing a mixture between the two parental copies. Moreover, by using large genomic windows (≥50kb) that likely span multiple independent loci, phylogenetic analyses in windows encompassed distinct phylogenetic signals, potentially leading to bias and inaccuracy in the inferences. Thawornwattana et al (2018) previously showed that this “concatenation approach”  could significantly impact phylogenetic inferences. They proposed instead to use loci small enough to minimise the risk of intra-locus recombination and to consider them in blocks of non-recombining loci along the genome in order to conduct phylogenetic analysed, ideally under the multi-species coalescent (MSC) that can account for ILS (e.g. BPP; Flouri et al. 2018; Jiao et al. 2020; Yang 2015). Such an approach applied to the diversification of the Delphinidae may reveal substantial changes compared to the currently admitted species tree.

Inaccuracy in the species tree estimation may have a major impact on the introgression analyses conducted in this study since the species tree and branching order must be supplied in the introgression analyses to properly disentangle introgression from ILS. Here, the authors rely on the tree topology that was previously estimated in McGowen et al. (2020), which they also recovered using their consensus estimation from ASTRAL-III (Zhang et al. 2018). While the methodologies accounted to a certain extent for ILS, albeit with potential bias induced by the concatenation approach, they ignore the presumably large amount of introgression among species during the diversification process. Estimating species branching order while ignoring introgression can lead to major bias in the phylogenetic inference and can lead to incorrect topologies. Even if these MSC-based methods account for ILS, inferences can become very inaccurate or even break down as gene flow increases (see for ex. Jiao et al. 2020; Müller et al. in press; Solís-Lemus et al. 2016). Dedicated approaches have been developed to model explicitly introgression together with ILS to estimate phylogenetic networks (Blair & Ané 2020; Rabier et al. 2021) or in isolation-with-migration model (Müller et al. in press; Wang et al. 2020). Future studies revisiting the reticulated evolutionary history of the Delphinoidae with such approaches may not only precise the species branching order, but also deliver a finer view of the magnitude and prevalence of introgression during the evolutionary history of these species.

A final part of Westbury et al. (2022)'s study set out to test whether historical periods of low abundance could have facilitated hybridization among Delphinoidae species. During these periods of low abundance, species may encounter only a limited number of conspecifics and may consider individuals from other species as suitable mating partners, leading to hybridisation (Crossman et al. 2016; Edwards et al. 2011; Westbury et al. 2019). The authors tested this hypothesis by considering genome-wide genetic diversity (or heterozygosity) as a proxy of historical effective population size (Ne), itself as a proxy of the evolution of census size with time. They also try to link historical Ne variation (from PSMC, Li & Durbin 2011) with their estimated time to cessation of gene flow or ILS (from the CRR of hPSMC). However, no straightforward relationship was found between the genetic diversity and the propensity of species to hybridize, nor was there any clear link between Ne variation through time and the cessation of gene flow or ILS. Such a lack of relationship may not come as a surprise, since the determinants of genome-wide genetic diversity and its variation through evolutionary time-scale are far more diverse and complex than just a direct link with hybridization, introgression, or even with the census population size. In fact, genetic diversity results from the balance between all the evolutionary processes at play in the species' evolutionary history (see the review of Ellegren & Galtier 2016). Other important factors can strongly impact genetic diversity, including demography and structure, but also linked selection (Boitard et al. 2022; Buffalo 2021; Ellegren & Galtier 2016). 

All in all, Westbury and coll. (2022) present here an interesting study providing an additional step towards resolving and understanding the complex evolutionary history of the Delphinoidae, and shedding light on the importance of introgression during the diversification of these cetacean species. Prospective work improving upon the taxonomic sampling, with additional genomic data for each species, considered with dedicated approaches tailored at estimating species tree or network while accounting for ILS and introgression will be key for refining the picture depicted in this study. Down the road, altogether these studies will contribute to assessing the evolutionary significance of introgression on the diversification of Delphinoides, and more generally on the diversification of cetacean species, which still remain an open and exciting perspective. 

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Flouri T, Jiao X, Rannala B, Yang Z (2018) Species Tree Inference with BPP Using Genomic Sequences and the Multispecies Coalescent. Mol Biol Evol 35, 2585-2593. https://doi.org/10.1093/molbev/msy147

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Tropical biodiversity is immense, under enormous threat, and yet still poorly understood. Global climatic breakdown and habitat destruction are impacting on and removing this diversity before we can understand how the biota responds to such changes, or even fully appreciate what we are losing [1]. This is particularly the case for woody shrubs and trees [2] and for the flora of tropical Africa [3].  

Helmstetter et al. [4] have taken a significant step to improve our understanding of African tropical tree diversity in the context of past climatic change. They have done so by means of a remarkably in-depth analysis of one species of the tropical plant family Annonaceae: Annickia affinis [5]. A. affinis shows a distribution pattern in Africa found in various plant (but interestingly not animal) groups: a discontinuity between north and south of the equator [6]. There is no obvious physical barrier to cause this discontinuity, but it does correspond with present day distinct northern and southern rainy seasons. Various explanations have been proposed for this discontinuity, set out as hypotheses to be tested in this paper: climatic fluctuations resulting in changes in plant distributions in the Pleistocene, or differences in flowering times or in ecological niche between northerly and southerly populations. These explanations are not mutually exclusive, but they can be tested using phylogenetic inference – if you can sample variable enough sequence data from enough individuals – complemented with analysis of ecological niches and traits.  

Using targeted sequence capture, the authors amassed a dataset representing 351 nuclear markers for 112 individuals of A. affinis. This dataset is impressive for a number of reasons: First, sampling such a species across such a wide range in tropical Africa presents numerous challenges of itself. Second, the technical achievement of using this still relatively new sequencing technique with a custom set of baits designed specifically for this plant family [7] is also considerable. The result is a volume of data that just a few years ago would not have been feasible to collect, and which now offers the possibility to meaningfully analyse DNA sequence variation within a species across numerous independent loci of the nuclear genome. This is the future of our research field, and the authors have ably demonstrated some of its possibilities.  

Using this data, they performed on the one hand different population genetic clustering approaches, and on the other, different phylogenetic inference methods. I would draw attention to their use and comparison of coalescence and network-based approaches, which can account for the differences between gene trees that might be expected between populations of a single species. The results revealed four clades and a consistent sequence of divergences between them. The authors inferred past shifts in geographic range (using a continuous state phylogeographic model), depicting a biogeographic scenario involving a dispersal north over the north/south discontinuity; and demographic history, inferring in some (but not all) lineages increases in effective population size around the time of the last glacial maximum, suggestive of expansion from refugia. Using georeferenced specimen data, they compared ecological niches between populations, discovering that overlap was indeed smallest comparing north to south. Just the phenology results were effectively inconclusive: far better data on flowering times is needed than can currently be harvested from digitised herbarium specimens.  

Overall, the results add to the body of evidence for the impact of Pleistocene climatic changes on population structure, and for niche differences contributing to the present day north/south discontinuity. However, they also paint a complex picture of idiosyncratic lineage-specific responses, even within a single species. With the increasing accessibility of the techniques used here we can look forward to more such detailed analyses of independent clades necessary to test and to expand on these conclusions, better to understand the nature of our tropical plant diversity while there is still opportunity to preserve it for future generations.  

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Parasites can manipulate their host’s behaviour to ensure their own transmission. These manipulated behaviours may be outside the range of ordinary host activities [1], or alter the crucial timing and/or location of a host’s regular activity. Vantaux et al show that the latter is true for the human malaria parasite, Plasmodium falciparum [2]. They demonstrate that three species of Anopheles mosquito were 24% more likely to choose human hosts, rather than other vertebrates, for their blood feed when they harboured transmissible stages (sporozoites) compared to when they were uninfected, or infected with non-transmissible malaria parasites [2]. Host choice is crucial for the malaria parasite Plasmodium falciparum to complete its life-cycle, as their host range is much narrower than the mosquito’s for feeding; P. falciparum can only develop in hominids, or closely related apes [3].
The study only shows this stage-dependent parasite manipulation retrospectively (by identifying host type and parasite stage in mosquitoes after their blood feed [2]). There was no difference in the preferences of infectious (with sporozoites) or un-infectious (infected without sporozoites, or uninfected) mosquitoes between human versus cow hosts in a choice test [2]. This suggests that the final decision about whether to feed occurs when the mosquito is in close range of the host.
This, coupled with previous findings, shows that vector manipulation is a fine-tuned business, that can act at multiple stages of the parasite life-cycle and on many behaviours [4]. Indeed, mosquitoes with non-transmissible Plasmodium stages (oocysts) are more reluctant to feed than sporozoite-infected mosquitoes [5] as vectors can be killed by their host whilst feeding, doing so before they are ready to transmit is risky for the malaria parasite. Thus, it seems that Plasmodium is, to some extent, master of its vector; commanding it not to feed when it cannot be transmitted, to feed when it is ready to be transmitted and to feed on the right type of host. What does this mean for our understanding of malaria transmission and epidemics?
Vantaux et al use a mathematical model, parameterised using data from this experiment, to highlight the consequences of this 24% increase in feeding on humans for P. falciparum transmission. They show that this increase raises the number of infectious bites humans receive from 4 (if sporozoite-infected mosquitoes had the same probability as uninfected mosquitoes) to 14 (an increase in 250%), for mosquitoes with a 15-day life-span, at ratios of 1:1 mosquitoes to humans. Longer mosquito life-spans and higher ratios of mosquitoes to humans further increases the number of infectious bites.
These results [2] have important implications for epidemiological forecasting and disease management. Public health strategies could focus on possible ways to trap sporozoite-infected mosquitoes, mimicking cues they use to locate their human hosts, or identify the behaviour of mosquitoes harbouring non-yet infectious Plasmodium, and trap them before they bite. Moreover, the results of the model show that failing to take into account the preference for humans of sporozoite-infected mosquitoes could underestimate the size of pending epidemics.
An important question previously raised is whether Plasmodium-induced alteration in host behaviour really is manipulation, or just a side-effect of being infected [4,5]. The fact that Vantaux et al show that these altered feeding behaviours increases the likelihood of transmission, in that a sporozoite-infected mosquito is more likely to feed on a human, strongly suggests that it is adaptive for the parasite [2]. Ultimately, to show that it is manipulation would require the identification of molecular factors released by Plasmodium that are responsible for physiological changes in the mosquito [6].

References

[1] Thomas, F., Schmidt-Rhaesa, A., Martin, G., Manu, C., Durand, P., & Renaud, F. (2002). Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts? Journal of Evolutionary Biology, 15(3), 356–361. doi: 10.1046/j.1420-9101.2002.00410.x
[2] Vantaux, A., Yao, F., Hien, D. F., Guissou, E., Yameogo, B. K., Gouagna, L.-C., … Lefevre, T. (2018). Field evidence for manipulation of mosquito host selection by the human malaria parasite, Plasmodium falciparum. BioRxiv, 207183 ver 6. doi: 10.1101/207183
[3] Prugnolle, F., Durand, P., Ollomo, B., Duval, L., Ariey, F., Arnathau, C., … Renaud, F. (2011). A Fresh Look at the Origin of Plasmodium falciparum, the Most Malignant Malaria Agent. PLOS Pathogens, 7(2), e1001283. doi: 10.1371/journal.ppat.1001283
[4] Cator, L. J., Lynch, P. A., Read, A. F., & Thomas, M. B. (2012). Do malaria parasites manipulate mosquitoes? Trends in Parasitology, 28(11), 466–470. doi: 10.1016/j.pt.2012.08.004
[5] Cator, L. J., George, J., Blanford, S., Murdock, C. C., Baker, T. C., Read, A. F., & Thomas, M. B. (2013). “Manipulation” without the parasite: altered feeding behaviour of mosquitoes is not dependent on infection with malaria parasites. Proceedings. Biological Sciences, 280(1763), 20130711. doi: 10.1098/rspb.2013.0711
[6] Herbison, R., Lagrue, C., & Poulin, R. (2018). The missing link in parasite manipulation of host behaviour. Parasites & Vectors, 11. doi: 10.1186/s13071-018-2805-9