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13 Dec 2016
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Addicted? Reduced host resistance in populations with defensive symbionts

Hooked on Wolbachia

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This very nice paper by Martinez et al. [1] provides further evidence, if further evidence was needed, of the extent to which heritable microorganisms run the evolutionary show.
Wolbachia is an ubiquitous endosymbiont of arthropods who has been recently shown to protect its hosts against viral infections. Here, Martinez et al. are able to show that this multifaceted heritable symbiont weakens selective pressures induced by viruses on host immune genes. In a series of very elegant experiments, Wolbachia-infected and Wolbachia-free populations of D. melanogaster were exposed to Drosophila C virus (a natural, and highly virulent Drosophila pathogen). At the end of a 9-generation artificial selection protocol with DCV, resistance against DCV increased in flies, both in the presence and absence of Wolbachia. Wolbachia-infected flies were still substantially more resistant to DCV viruses than their Wolbachia-free counterparts. Crucially, however, the frequency of the pastrel resistant allele (a key immune gene for DCV resistance) was significantly lower in the Wolbachia-infected lines. As a consequence, when the DCV-evolved lines were treated with antibiotics to cure them from the bacterial infection, the lines who had evolved with Wolbachia tended to be more susceptible to the virus than their uninfected counterparts.
In other words, infection by protective heritable symbionts can affect how selection acts on the host's nuclear-based resistance, effectively rendering it dependent on its symbiont for the fight against pathogens.
But the interest of these results may not be simply academic. The protective qualities of Wolbachia against a range of pathogens have opened up the exciting possibility of transferring these bacteria to mosquito vectors of key human diseases such as dengue or malaria. The long term evolutionary potential for these novel Wolbachia-host interactions has, however, been little explored. Either the Wolbachia, the pathogen or, as shown here, the host, could evolve in more or less predictable ways. There is, for example, evidence showing that in novel hosts Wolbachia evolves rapidly and tends to gradually lose its virulence. If the lost virulence was to result in a decrease in their pathogen defensive qualities, the mosquito, having lost the efficiency of its conventional immune defences, could end up being more vulnerable to infection than before the Wolbachia introduction. Martinez et al.'s paper is a nice example of how investigating the evolutionary potential of such Wolbachia-host-pathogen interactions can be hugely informative as to the long term prospects of these new control methods.


[1] Martinez J, Cogni R, Cao C, Smith S, Illingworth CJR & Jiggins FM. 2016. Addicted? Reduced host resistance in populations with defensive symbionts. Proceedings of the Royal Society of London B 283:20160778. doi: 10.1098/rspb.2016.0778

Addicted? Reduced host resistance in populations with defensive symbiontsMartinez J, Cogni R, Cao C, Smith S, Illingworth CJR & Jiggins FMHeritable symbionts that protect their hosts from pathogens have been described in a wide range of insect species. By reducing the incidence or severity of infection, these symbionts have the potential to reduce the strength of selection on genes ...Adaptation, Evolutionary Applications, Evolutionary Ecology, Experimental Evolution, Life HistoryAna Rivero2016-12-13 20:08:37 View
16 Mar 2017
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Correlated paternity measures mate monopolization and scales with the magnitude of sexual selection

Measurement of sexual selection in plants made easier

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Sexual selection occurs in flowering plants too. However it tends to be understudied in comparison to animal sexual selection, in part because the minuscule size and long dispersal distances of the individuals producing male gametes (pollen grains) seriously complicate the estimation of male siring success and thereby the measurement of sexual selection. Dorken and Perry [1] introduce a novel and clever approach to estimate sexual selection in plants, which bypasses the need for a direct quantification of absolute male mating success. This approach builds on the fact that the strength of sexual selection is directly related to the ability of individuals to monopolize mates [2]. In plants, mate monopolization can be assessed by examining the proportion of seeds produced by a given plant that are full-sibs, i.e. that share the same father. A nice feature of this proportion of full-sib seeds per maternal parent is it equals the coefficient of correlated paternity of Ritland [3], which can be readily obtained from the hundreds of plant mating system studies using genetic markers. A less desirable feature of the proportion of full sibs per maternal plant is that it is inversely related to population size, an effect that should be corrected for. The resulting index of mate monopolization is a simple product: (coefficient of correlated paternity)x(population size – 1). The authors test whether their index of mate monopolization is a good correlate of sexual selection, measured more traditionally as the selection differential on a trait influencing mating success, using a combination of theoretical and experimental approaches. Both approaches confirm that the two quantities are positively correlated, which suggests that the index of mate monopolization could be a convenient way to estimate the relative strength of sexual selection in flowering plants. These results call for further investigation, e.g. to verify that the effect of population size is well controlled for, or to assess the effects of non-random mating and inbreeding depression; however, this work paves the way for an expansion of sexual selection studies in flowering plants.


[1] Dorken ME and Perry LE. 2017. Correlated paternity measures mate monopolization and scales with the magnitude of sexual selection. Journal of Evolutionary Biology 30: 377-387 doi: 10.1111/jeb.13013

[2] Klug H, Heuschele J, Jennions M and Kokko H. 2010. The mismeasurement of sexual selection. Journal of Evolutionary Biology 23:447-462. doi: 10.1111/j.1420-9101.2009.01921.x

[3] Ritland K. 1989. Correlated matings in the partial selfer Mimulus guttatus. Evolution 43:848-859. doi: 10.2307/2409312

Correlated paternity measures mate monopolization and scales with the magnitude of sexual selectionDorken, ME and Perry LEIndirect measures of sexual selection have been criticized because they can overestimate the magnitude of selection. In particular, they do not account for the degree to which mating opportunities can be monopolized by individuals of the sex that ...Sexual SelectionEmmanuelle Porcher2017-03-13 23:22:26 View
07 Nov 2017
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MaxTiC: Fast ranking of a phylogenetic tree by Maximum Time Consistency with lateral gene transfers

Dating nodes in a phylogeny using inferred horizontal gene transfers

Recommended by and based on reviews by Alexandros Stamatakis, Mukul Bansal and 2 anonymous reviewers

Dating nodes in a phylogeny is an important problem in evolution and is typically performed by using molecular clocks and fossil age estimates [1]. The manuscript by Chauve et al. [2] reports a novel method, which uses lateral gene transfers to help ordering nodes in a species tree. The idea is that a lateral gene transfer can only occur between two species living at the same time, which indirectly informs on node relative ages in a phylogeny: the donor species cannot be more recent than the recipient species. Horizontal gene transfers are increasingly recognized as frequent, even in eukaryotes, and especially in micro-organisms that have little fossil records [3-7]. Yet, such an important source of information has been very rarely used so far for inferring relative node ages in phylogenies. In this context, the method by Chauve et al. [2] represents an innovative and original approach to a difficult problem. An obvious limitation of the approach is that it relies on inferences of horizontal transfers, which detection is in itself a difficult problem. Incomplete taxon sampling, or the extinction of the true donor lineage may render patterns difficult to interpret in a temporary fashion. Yet, for clades with no fossils this may be the only piece of information we have at hand, and the growing amount of sequence data is likely to minimize issues derived from incomplete sampling.

The developed method, MaxTiC (for Maximal Time Consistency) [2], represents a very nice application of theoretical developments on the well-known « Feedback Arc Set » computer science problem to the evolutionary question of ordering nodes in a phylogeny. MaxTiC uses as input a species tree and a set of time constraints based on lateral gene transfers inferred using other softwares, and minimizes conflicts between node ordering and these time constraints. The application of MaxTiC on simulated datasets indicated that node ordering was fairly accurate [2]. MaxTiC is implemented in a freely available software, which represents original and relevant contribution to the field of evolutionary biology.


[1] Donoghue P and Smith M, editors. 2003. Telling the evolutionary time. CRC press.

[2] Chauve C, Rafiey A, Davin AA, Scornavacca C, Veber P, Boussau B, Szöllősi GJ, Daubin V and Tannier E. 2017. MaxTiC: Fast ranking of a phylogenetic tree by Maximum Time Consistency with lateral gene transfers. bioRxiv 127548, ver. 6 of 6th November 2017. doi: 10.1101/127548

[3] Ropars J, Rodríguez de la Vega RC, Lopez-Villavicencio M, Gouzy J, Sallet E, Debuchy R, Dupont J, Branca A and Giraud T. 2015. Adaptive horizontal gene transfers between multiple cheese-associated fungi. Current Biology 19, 2562–2569. doi: 10.1016/j.cub.2015.08.025

[4] Novo M, Bigey F, Beyne E, Galeote V, Gavory F, Mallet S, Cambon B, Legras JL, Wincker P, Casaregola S and Dequin S. 2009. Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118. Proceeding of the National Academy of Science USA, 106, 16333–16338. doi: 10.1073/pnas.0904673106

[5] Naranjo-Ortíz MA, Brock M, Brunke S, Hube B, Marcet-Houben M, Gabaldón T. 2016. Widespread inter- and intra-domain horizontal gene transfer of d-amino acid metabolism enzymes in Eukaryotes. Frontiers in Microbiology 7, 2001. doi: 10.3389/fmicb.2016.02001

[6] Alexander WG, Wisecaver JH, Rokas A, Hittinger CT. 2016. Horizontally acquired genes in early-diverging pathogenic fungi enable the use of host nucleosides and nucleotides. Proceeding of the National Academy of Science USA. 113, 4116–4121. doi: 10.1073/pnas.1517242113

[7] Marcet-Houben M, Gabaldón T. 2010. Acquisition of prokaryotic genes by fungal genomes. Trends in Genetics. 26, 5–8. doi: 10.1016/j.tig.2009.11.007

MaxTiC: Fast ranking of a phylogenetic tree by Maximum Time Consistency with lateral gene transfersCédric Chauve, Akbar Rafiey, Adrian A. Davin, Celine Scornavacca, Philippe Veber, Bastien Boussau, Gergely J Szöllosi, Vincent Daubin, and Eric TannierLateral gene transfers (LGTs) between ancient species contain information about the relative timing of species diversification. Specifically, the ancestors of a donor species must have existed before the descendants of the recipient species. Hence...Bioinformatics & Computational Biology, Evolutionary Dynamics, Genome Evolution, Life History, Molecular Evolution, Phylogenetics / PhylogenomicsTatiana Giraud2017-06-28 13:40:52 View
10 Nov 2017
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Rates of Molecular Evolution Suggest Natural History of Life History Traits and a Post-K-Pg Nocturnal Bottleneck of Placentals

A new approach to DNA-aided ancestral trait reconstruction in mammals

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Reconstructing ancestral character states is an exciting but difficult problem. The fossil record carries a great deal of information, but it is incomplete and not always easy to connect to data from modern species. Alternatively, ancestral states can be estimated by modelling trait evolution across a phylogeny, and fitting to values observed in extant species. This approach, however, is heavily dependent on the underlying assumptions, and typically results in wide confidence intervals.

An alternative approach is to gain information on ancestral character states from DNA sequence data. This can be done directly when the trait of interest is known to be determined by a single, or a small number, of major effect genes. In some of these cases it can even be possible to investigate an ancestral trait of interest by inferring and resurrecting ancestral sequences in the laboratory. Examples where this has been successfully used to address evolutionary questions range from the nocturnality of early mammals [1], to the loss of functional uricases in primates, leading to high rates of gout, obesity and hypertension in present day humans [2]. Another possibility is to rely on correlations between species traits and the genome average substitution rate/process. For instance, it is well established that the ratio of nonsynonymous to synonymous substitution rate, dN/dS, is generally higher in large than in small species of mammals, presumably due to a reduced effective population size in the former. By estimating ancestral dN/dS, one can therefore gain information on ancestral body mass (e.g. [3-4]).

The interesting paper by Wu et al. [5] further develops this second possibility of incorporating information on rate variation derived from genomic data in the estimation of ancestral traits. The authors analyse a large set of 1185 genes in 89 species of mammals, without any prior information on gene function. The substitution rate is estimated for each gene and each branch of the mammalian tree, and taken as an indicator of the selective constraint applying to a specific gene in a specific lineage – more constraint, slower evolution. Rate variation is modelled as resulting from a gene effect, a branch effect, and a gene X branch interaction effect, which captures lineage-specific peculiarities in the distribution of functional constraint across genes. The interaction term in terminal branches is regressed to observed trait values, and the relationship is used to predict ancestral traits from interaction terms in internal branches. The power and accuracy of the estimates are convincingly assessed via cross validation. Using this method, the authors were also able to use an unbiased approach to determine which genes were the main contributors to the evolution of the life-history traits they reconstructed.

The ancestors to current placental mammals are predicted to have been insectivorous - meaning that the estimated distribution of selective constraint across genes in basal branches of the tree resembles that of extant insectivorous taxa - consistent with the mainstream palaeontological hypothesis. Another interesting result is the prediction that only nocturnal lineages have passed the Cretaceous/Tertiary boundary, so that the ancestors of current orders of placentals would all have been nocturnal. This suggests that the so-called "nocturnal bottleneck hypothesis" should probably be amended. Similar reconstructions are achieved for seasonality, sociality and monogamy – with variable levels of uncertainty.

The beauty of the approach is to analyse the variance, not only the mean, of substitution rate across genes, and their methods allow for the identification of the genes contributing to trait evolution without relying on functional annotations. This paper only analyses discrete traits, but the framework can probably be extended to continuous traits as well.


[1] Bickelmann C, Morrow JM, Du J, Schott RK, van Hazel I, Lim S, Müller J, Chang BSW, 2015. The molecular origin and evolution of dim-light vision in mammals. Evolution 69: 2995-3003. doi:

[2] Kratzer, JT, Lanaspa MA, Murphy MN, Cicerchi C, Graves CL, Tipton PA, Ortlund EA, Johnson RJ, Gaucher EA, 2014. Evolutionary history and metabolic insights of ancient mammalian uricases. Proceedings of the National Academy of Science, USA 111:3763-3768. doi:

[3] Lartillot N, Delsuc F. 2012. Joint reconstruction of divergence times and life-history evolution in placental mammals using a phylogenetic covariance model. Evolution 66:1773-1787. doi:

[4] Romiguier J, Ranwez V, Douzery EJ, Galtier N. 2013. Genomic evidence for large, long-lived ancestors to placental mammals. Molecular Biology and Evolution 30:5-13. doi:

[5] Wu J, Yonezawa T, Kishino H. 2016. Rates of Molecular Evolution Suggest Natural History of Life History Traits and a Post-K-Pg Nocturnal Bottleneck of Placentals. Current Biology 27: 3025-3033. doi:

Rates of Molecular Evolution Suggest Natural History of Life History Traits and a Post-K-Pg Nocturnal Bottleneck of PlacentalsWu J, Yonezawa T, Kishino H.Life history and behavioral traits are often difficult to discern from the fossil record, but evolutionary rates of genes and their changes over time can be inferred from extant genomic data. Under the neutral theory, molecular evolutionary rate i...Bioinformatics & Computational Biology, Life History, Molecular Evolution, Paleontology, Phylogenetics / PhylogenomicsNicolas Galtier2017-11-10 14:52:26 View
20 Dec 2016
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Experimental Evolution of Gene Expression and Plasticity in Alternative Selective Regimes

Genetic adaptation counters phenotypic plasticity in experimental evolution

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How do phenotypic plasticity and adaptive evolution interact in a novel or changing environment? Does evolution by natural selection generally reinforce initially plastic phenotypic responses, or does it instead oppose them? And to what extent does evolution of a trait involve evolution of its plasticity? These questions have lied at the heart of research on phenotypic evolution in heterogeneous environments ever since it was realized that the environment is likely to affect the expression of many (perhaps most) characters of an individual. Importantly, this broad definition of phenotypic plasticity as change in the average phenotype of a given genotype in response to its environment of development (or expression) does not involve any statement about the adaptiveness of the plastic changes. Theory on the evolution of plasticity has devoted much effort to understanding how reaction norm should evolve under different regimes of environmental change in space and time, and depending on genetic constraints on reaction norm shapes. However on an empirically ground, the questions above have mostly been addressed for individual traits, often chosen a priori for their likeliness to exhibit adaptive plasticity, and we still lack more systematic answers. These can be provided by so-called ‘phenomic’ approaches, where a large number of traits are tracked without prior information on their biological or ecological function. A problem is that the number of phenotypic characters that can be measured in an organism is virtually infinite (and to some extent arbitrary), and that scaling issues makes it difficult to compare different sets of traits. Gene-expression levels offer a partial solution to this dilemma, as they can be considered as a very large number of traits (one per typed gene) that can be measured easily and uniformly (fold change in the number of reads in RNAseq). As for any traits, expression levels of different genes may be genetically correlated, to an extent that depends on their regulation mechanism: cis-regulatory sequences that only affect expression of neighboring genes are likely to cause independent gene expression, while more systematic modifiers of expression (e.g. trans-regulators such as transcription factors) may cause correlated genetic responses of the expression of many genes. Huang and Agrawal [1] have studied plasticity and evolution of gene expression level in young larvae of populations of Drosophila melanogaster that have evolved for about 130 generations under either a constant environment (salt or cadmium), or an environment that is heterogeneous in time or space (combining salt and cadmium). They report a wealth of results, of which we summarize the most striking here. First, among genes that (i) were initially highly plastic and (ii) evolved significant divergence in expression levels between constant environment treatments, the evolved divergence is predominantly in the opposite direction to the initial plastic response. This suggests that either plasticity was initially maladaptive, or the selective pressure changed during the evolutionary process (see below). This somewhat unexpected result strikingly mirrors that from a study published last year in Nature [2], where the same pattern was found for responses of guppies to the presence of predators. However, Huang and Agrawal [1] went beyond this study by deciphering the underlying mechanisms in several interesting ways. First, they showed that change in gene expression often occurred at genes close to SNPs with differentiated frequencies across treatments (but not at genes with differentiated SNPs in their coding sequences), suggesting that cis-regulatory sequences are involved. This is also suggested by the fact that changes in gene expression are mostly caused by the increased expression of only one allele at polymorphic loci, and is a first step towards investigating the genetic underpinnings of (co)variation in gene expression levels. Another interesting set of findings concerns evolution of plasticity in treatments with variable environments. To compare the gene-expression plasticity that evolved in these treatments to an expectation, the authors considered that the expression levels in populations maintained for a long time under constant salt or cadmium had reached an optimum. The differences between these expression levels were thus assumed to predict the level of plasticity that should evolve in a heterogeneous environment (with both cadmium and salt) under perfect environmental predictability. The authors showed that plasticity did evolve more in the expected direction in heterogeneous than in constant environments, resulting in better adapted final expression levels across environments. Taken collectively, these results provide an unprecedented set of patterns that are greatly informative on how plasticity and evolution interact in constant versus changing environments. But of course, interpretations in terms of adaptive versus maladaptive plasticity are more challenging, as the authors themselves admit. Even though environmentally determined gene expression is the basic mechanism underlying the phenotypic plasticity of most traits, it is extremely difficult to relate to more integrated phenotypes for which we can understand the selection pressures, especially in multicellular organisms. The authors have recently investigated evolutionary change of quantitative traits in these selected lines, so it might be possible to establish links between reaction norms for macroscopic traits to those for gene expression levels. Such an approach would also involve tracking gene expression throughout life, rather than only in young larvae as done here, thus putting phenotypic complexity back in the picture also for expression levels. Another difficulty is that a plastic response that was originally adaptive may be replaced by an opposite evolutionary response in the long run, without having to invoke initially maladaptive plasticity. For instance, the authors mention the possibility that a generic stress response is initially triggered by cadmium, but is eventually unnecessary and costly after evolution of genetic mechanisms for cadmium detoxification (a case of so-called genetic accommodation). In any case, this study by Huang and Agrawal [1], together with the one by Ghalambor et al. last year [2], reports novel and unexpected results, which are likely to stimulate researchers interested in plasticity and evolution in heterogeneous environments for the years to come.


[1] Huang Y, Agrawal AF. 2016. Experimental Evolution of Gene Expression and Plasticity in Alternative Selective Regimes. PLoS Genetics 12:e1006336. doi: 10.1371/journal.pgen.1006336

[2] Ghalambor CK, Hoke KL, Ruell EW, Fischer EK, Reznick DN, Hughes KA. 2015. Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature. Nature 525: 372-375. doi: 10.1038/nature15256

Experimental Evolution of Gene Expression and Plasticity in Alternative Selective RegimesHuang Y, Agrawal AFLittle is known of how gene expression and its plasticity evolves as populations adapt to different environmental regimes. Expression is expected to evolve adaptively in all populations but only those populations experiencing environmental heterog...Adaptation, Experimental Evolution, Expression Studies, Phenotypic PlasticityLuis-Miguel Chevin2016-12-20 09:04:15 View
18 Dec 2017
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Co-evolution of virulence and immunosuppression in multiple infections

Two parasites, virulence and immunosuppression: how does the whole thing evolve?

Recommended by based on reviews by 2 anonymous reviewers

How parasite virulence evolves is arguably the most important question in both the applied and fundamental study of host-parasite interactions. Typically, this research area has been progressing through the formalization of the problem via mathematical modelling. This is because the question is a complex one, as virulence is both affected and affects several aspects of the host-parasite interaction. Moreover, the evolution of virulence is a problem in which ecology (epidemiology) and evolution (changes in trait values through time) are tightly intertwined, generating what is now known as eco-evolutionary dynamics. Therefore, intuition is not sufficient to address how virulence may evolve.
In their classical model, Anderson and May [1] predict that the optimal virulence level results from a trade-off between increasing parasite load within hosts and promoting transmission between hosts. Although very useful and foundational, this model incurs into several simplifying assumptions. One of the most obvious is that it considers that hosts are infected by a single parasite strain/species. Some subsequent models have thus accounted for multiple infections, generally predicting that this will select for higher virulence, because it increases the strength of selection in the within-host compartment.
Usually, when attacked, hosts deploy defences to combat their parasites. In many systems, however, parasites can suppress the immune response of their hosts. This leads to prolonged infection, which is beneficial for the parasite. However, immunosuppressed hosts are also more prone to infection. Thus, multiple infections are more likely in a population of immunosuppressed hosts, leading to higher virulence, hence a shorter infection period. Thus, the consequences of immunosuppression for the evolution of virulence in a system allowing for multiple infections are not straightforward.
Kamiya et al.[2] embrace this challenge. They create an epidemiological model in which the probability of co-infection trades off with the rate of recovery from infection, via immunosuppression. They then use adaptive dynamics to study how either immunosuppression or virulence evolve in response to one another, to then establish what happens when they both coevolve. They find that when virulence only evolves, its evolutionary equilibrium increases as immunosuppression levels increase. In the reverse case, that is, when virulence is set to a fixed value, the evolutionarily stable immunosuppression varies non-linearly with virulence, with first a decrease, but then an increase at high levels of virulence. The initial decrease of immunosuppression may be due to (a) a decrease in infection duration and/or (b) a decrease in the proportion of double infections, caused by increased levels of virulence. However, as virulence increases, the probability of double infections decreases even in non-immunosuppressed hosts, hence increased immunosuppression is selected for.
The combination of both Evolutionary Stable Strategies (ESSs) yields intermediate levels of virulence and immunosuppression. The authors then address how this co-ESS varies with host mortality and with the shape of the trade-off between the probability of co-infection and the rate of recovery. They find that immunosuppression always decreases with increased host mortality, as it becomes not profitable to invest on this trait. In contrast, virulence peaks at intermediate values of host mortality, unlike the monotonical decrease that is found in absence of immunosuppression. Also, this relationship is predicted to vary with the shape of the trade-off underlying the costs and benefits of immunosuppression.
In sum, Kamiya et al. [2] provide a comprehensive analysis of an important problem in the evolution of host-parasite interactions. The model provides clear predictions, and thus can now be tested using the many systems in which immunosuppression has been detected, provided that the traits that compose the model can be measured.


[1] Anderson RM and May RM. 1982. Coevolution of hosts and parasites. Parasitology, 1982. 85: 411–426. doi: 10.1017/S0031182000055360

[2] Kamiya T, Mideo N and Alizon S. 2017. Coevolution of virulence and immunosuppression in multiple infections. bioRxiv, ver. 7 peer-reviewed by PCI Evol Biol, 149211. doi: 10.1101/139147

Co-evolution of virulence and immunosuppression in multiple infectionsTsukushi Kamiya, Nicole Mideo, Samuel AlizonMany components of the host-parasite interaction have been shown to affect the way virulence, that is parasite induced harm to the host, evolves. However, co-evolution of multiple traits is often neglected. We explore how an immunosuppressive mech...Evolutionary Applications, Evolutionary Dynamics, Evolutionary Ecology, Evolutionary Epidemiology, Evolutionary TheorySara Magalhaes2017-06-13 16:49:45 View
29 Sep 2017
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Parallel diversifications of Cremastosperma and Mosannona (Annonaceae), tropical rainforest trees tracking Neogene upheaval of the South American continent

Unravelling the history of Neotropical plant diversification

Recommended by based on reviews by Thomas Couvreur and Hervé Sauquet

South American rainforests, particularly the Tropical Andes, have been recognized as the hottest spot of plant biodiversity on Earth, while facing unprecedented threats from human impact [1,2]. Considerable research efforts have recently focused on unravelling the complex geological, bioclimatic, and biogeographic history of the region [3,4]. While many studies have addressed the question of Neotropical plant diversification using parametric methods to reconstruct ancestral areas and patterns of dispersal, Pirie et al. [5] take a distinct, complementary approach. Based on a new, near-complete molecular phylogeny of two Neotropical genera of the flowering plant family Annonaceae, the authors modelled the ecological niche of each species and reconstructed the history of niche differentiation across the region. The main conclusion is that, despite similar current distributions and close phylogenetic distance, the two genera experienced rather distinct processes of diversification, responding differently to the major geological events marking the history of the region in the last 20 million years (Andean uplift, drainage of Lake Pebas, and closure of the Panama Isthmus).

As a researcher who has not personally worked on Neotropical biogeography, I found this paper captivating and especially enjoyed very much reading the Introduction, which sets out the questions very clearly. The strength of this paper is the near-complete diversity of species the authors were able to sample in each clade and the high-quality data compiled for the niche models. I would recommend this paper as a nice example of a phylogenetic study aimed at unravelling the detailed history of Neotropical plant diversification. While large, synthetic meta-analyses of many clades should continue to seek general patterns [4,6], careful studies restricted on smaller, but well controlled and sampled datasets such as this one are essential to really understand tropical plant diversification in all its complexity.


[1] Antonelli A, and Sanmartín I. 2011. Why are there so many plant species in the Neotropics? Taxon 60, 403–414.

[2] Mittermeier RA, Robles-Gil P, Hoffmann M, Pilgrim JD, Brooks TB, Mittermeier CG, Lamoreux JL and Fonseca GAB. 2004. Hotspots revisited: Earths biologically richest and most endangered ecoregions. CEMEX, Mexico City, Mexico 390pp

[3] Antonelli A, Nylander JAA, Persson C and Sanmartín I. 2009. Tracing the impact of the Andean uplift on Neotropical plant evolution. Proceedings of the National Academy of Science of the USA 106, 9749–9754. doi: 10.1073/pnas.0811421106

[4] Hoorn C, Wesselingh FP, ter Steege H, Bermudez MA, Mora A, Sevink J, Sanmartín I, Sanchez-Meseguer A, Anderson CL, Figueiredo JP, Jaramillo C, Riff D, Negri FR, Hooghiemstra H, Lundberg J, Stadler T, Särkinen T and Antonelli A. 2010. Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330, 927–931. doi: 10.1126/science.1194585

[5] Pirie MD, Maas PJM, Wilschut R, Melchers-Sharrott H and Chatrou L. 2017. Parallel diversifications of Cremastosperma and Mosannona (Annonaceae), tropical rainforest trees tracking Neogene upheaval of the South American continent. bioRxiv, 141127, ver. 3 of 28th Sept 2017. doi: 10.1101/141127

[6] Bacon CD, Silvestro D, Jaramillo C, Tilston Smith B, Chakrabartye P and Antonelli A. 2015. Biological evidence supports an early and complex emergence of the Isthmus of Panama. Proceedings of the National Academy of Science of the USA 112, 6110–6115. doi: 10.1073/pnas.1423853112

Parallel diversifications of Cremastosperma and Mosannona (Annonaceae), tropical rainforest trees tracking Neogene upheaval of the South American continentMichael D. Pirie, Paul J. M. Maas, Rutger A. Wilschut, Heleen Melchers-Sharrott & Lars W. ChatrouMuch of the immense present day biological diversity of Neotropical rainforests originated from the Miocene onwards, a period of geological and ecological upheaval in South America. We assess the impact of the Andean orogeny, drainage of lake Peba...Phylogenetics / Phylogenomics, Phylogeography & BiogeographyHervé Sauquet Hervé Sauquet, Thomas Couvreur2017-06-03 21:25:48 View
14 Dec 2016
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High Rates of Species Accumulation in Animals with Bioluminescent Courtship Displays

Bioluminescent sexually selected traits as an engine for biodiversity across animal species

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In evolutionary biology, sexual selection is hypothesized to increase speciation rates in animals, as theory predicts that sexual selection will contribute to phenotypic diversification and affect rates of species accumulation at macro-evolutionary time scales. However, testing this hypothesis and gathering convincing evidence have proven difficult. Although some studies have shown a strong correlation between proxies of sexual selection and species diversity (mostly in birds), this relationship relies on some assumptions on the link between these proxies and the strength of sexual selection and is not detected in some other taxa, making taxonomically widespread conclusions impossible.

In a recent study published in Current Biology [1], Ellis and Oakley provide strong evidence that bioluminescent sexual displays have driven high species richness in taxonomically diverse animal lineages, providing a crucial link between sexual selection and speciation.
It was known that bioluminescence has evolved independently more than 40 times, with males often using it as a mating signal but with also some other possible adaptive functions including anti-predator defense and predation. Moreover, it has been reported that small marine lanternfishes and sharks that use bioluminescence in mate identification had a greater concentration of species than other deep-sea fishes that use bioluminescence for defensive purposes [2-4]. But no one had ever determined whether this pattern is consistent across diverse and distantly related animal groups living on sea and land.

Ellis and Oakley [1] explored the scientific literature for well-resolved evolutionary trees with branches containing bioluminescent lineages and identified lineages that use light for courtship or camouflage in a wide range of marine and terrestrial taxa including insects, crustaceans, cephalopods, segmented worms, and fishes. The researchers counted the number of species in each bioluminescent clade and found that all groups with light-courtship displays had more species and faster rates of species accumulation than their non-luminous most closely related sister lineages or ancestors. In contrast, those groups that used bioluminescence for predator avoidance had a lower than expected rate of species richness on average.

Nicely encompassing a diversity of taxa and neatly controlling for the rate of species accumulation of the encompassing clade, the results of Ellis and Oakley are clear-cut and provide the most comprehensive evidence to date for the hypothesis that sexual displays can act as drivers of speciation. One question this study incites is what is happening in terms of sexual selection in species displaying defensive bioluminescence or no bioluminescence at all: do those lineages use no mating signals at all or other mating signals that are less apparent, and will those experience lower levels of sexual selection than bioluminescent mating signals, i.e. consistent with Ellis and Oakley results? It would also be interesting to investigate the diversification rates in animal species using other modalities, such as chemical, acoustic or any other type of signals used by males, females or both sexes, to determine what types of sexual signals may be more generally drivers of speciation.


[1] Ellis EA, Oakley TH. 2016. High Rates of Species Accumulation in Animals with Bioluminescent Courtship Displays. Current Biology 26:1916–1921. doi: 10.1016/j.cub.2016.05.043

[2] Davis MP, Holcroft NI, Wiley EO, Sparks JS, Smith WL. 2014. Species-specific bioluminescence facilitates speciation in the deep sea. Marine Biology 161:1139­1148. doi: 10.1007/s00227-014-2406-x

[3] Davis MP, Sparks JS, Smith WL. 2016. Repeated and Widespread Evolution of Bioluminescence in Marine Fishes. PLoS One 11:e0155154. doi: 10.1371/journal.pone.0155154

[4] Claes JM, Nilsson D-E, Mallefet J, Straube N. 2015. The presence of lateral photophores correlates with increased speciation in deep-sea bioluminescent sharks. Royal Society Open Science 2:150219. doi: 10.1098/rsos.150219

High Rates of Species Accumulation in Animals with Bioluminescent Courtship DisplaysEllis EA, Oakley THOne of the great mysteries of evolutionary biology is why closely related lineages accumulate species at different rates. Theory predicts that populations undergoing strong sexual selection will more quickly differentiate because of increased pote...Adaptation, Evolutionary Ecology, Sexual Selection, SpeciationAstrid Groot2016-12-14 19:01:59 View
24 Oct 2022
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Evolutionary responses of energy metabolism, development, and reproduction to artificial selection for increasing heat tolerance in Drosophila subobscura

The other side of the evolution of heat tolerance: correlated responses in metabolism and life-history traits

Recommended by and based on reviews by Marija Savić Veselinović and 1 anonymous reviewer

Understanding how species respond to environmental changes is becoming increasingly important in order to predict the future of biodiversity and species distributions under current global warming conditions (Rezende 2020; Bennett et al 2021). Two key factors to take into account in these predictions are the tolerance of organisms to heat stress and subsequently how they adapt to increasingly warmer temperatures. Coupled with this, one important factor that is often overlooked when addressing the evolution of thermal tolerance, is the correlated responses in traits that are important to fitness, such as life histories, behavior and the underlying metabolic processes.

The rate and intensity of the thermal stress are expected to be major factors in shaping the evolution of heat tolerance and correlated responses in other traits. For instance, lower rates of thermal stress are predicted to select for individuals with a slower metabolism (Santos et al 2012), whereas low metabolism is expected to lead to a lower reproductive rate (Dammhahn et al 2018). To quantify the importance of the rate and intensity of thermal stress on the evolutionary response of heat tolerance and correlated response in behavior, Mesas et al (2021) performed experimental evolution in Drosophila subobscura using selective regimes with slow or fast ramping protocols. Whereas both regimes showed increased heat tolerance with similar evolutionary rates, the correlated responses in thermal performance curves for locomotor behavior differed between selection regimes. These findings suggest that thermal rate and intensity may shape the evolution of correlated responses in other traits, urging the need to understand possible correlated responses at relevant levels such as life history and metabolism. 

In the present contribution, Mesas and Castañeda (2022) investigate whether the disparity in thermal performance curves observed in the previous experiment (Mesas et al 2021) could be explained by differences in metabolic energy production and consumption, and how this correlated with the reproductive output (fecundity and viability). Overall, the authors show some evidence for lowered enzyme activity and increased performance in life-history traits, particularly for the slow-ramping selected flies. Specifically, the authors observe a reduction in glucose metabolism and increased viability when evolving under slow ramping stress. Interestingly, both regimes show a general increase in fecundity, suggesting that adaptation to these higher temperatures is not costly (for reproduction) in the ancestral environment. The evidence for a somewhat lower metabolism in the slow-ramping lines suggests the evolution of a slow “pace of life”. The “pace of life” concept tries to bridge variation across several levels namely metabolism, physiology, behavior and life history, with low “pace of life” organisms presenting lower metabolic rates, later reproduction and higher longevity than fast “pace of life” organisms (Dammhahn et al 2018, Tuzun & Stocks 2022).  As the authors state there is not a clear-cut association with the expectations of the pace of life hypothesis since there was evidence for increased reproductive output under both selection intensity regimes. This suggests that, given sufficient trait genetic variance, positively correlated responses may emerge during some stages of thermal evolution. As fecundity estimates in this study were focussed on early life, the possibility of a decrease in the cumulative reproductive output of the selected flies, even under benign conditions, cannot be excluded. This would help explain the apparent paradox of increased fecundity in selected lines. In this context, it would also be interesting to explore the variation in reproductive output at different temperatures, i.e to obtain thermal performance curves for life histories. 

Mesas and Castañeda (2022) raise important questions to pursue in the future and contribute to the growing evidence that, in order to predict the distribution of ectothermic species under current global warming conditions, we need to expand beyond determining the physiological thermal limits of each organism (Parratt et al 2021). Ultimately, integrating metabolic, life-history and behavioral changes during evolution under different thermal stresses within a coherent framework is key to developing better predictions of temperature effects on natural populations.  


Bennett, J.M., Sunday, J., Calosi, P. et al. The evolution of critical thermal limits of life on Earth. Nat Commun 12, 1198 (2021).

Dammhahn, M., Dingemanse, N.J., Niemelä, P.T. et al. Pace-of-life syndromes: a framework for the adaptive integration of behaviour, physiology and life history. Behav Ecol Sociobiol 72, 62 (2018).

Mesas, A,  Jaramillo, A,  Castañeda, LE.  Experimental evolution on heat tolerance and thermal performance curves under contrasting thermal selection in Drosophila subobscura. J Evol Biol  34, 767– 778 (2021).

Mesas, A, Castañeda, LE Evolutionary responses of energy metabolism, development, and reproduction to artificial selection for increasing heat tolerance in Drosophila subobscura. bioRxiv, 2022.02.03.479001, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology.

Parratt, S.R., Walsh, B.S., Metelmann, S. et al. Temperatures that sterilize males better match global species distributions than lethal temperatures. Nat. Clim. Chang. 11, 481–484 (2021).

Santos, M, Castañeda, LE, Rezende, EL Keeping pace with climate change: what is wrong with the evolutionary potential of upper thermal limits? Ecology and evolution, 2(11), 2866-2880 (2012).

Tüzün, N, Stoks, R. A fast pace-of-life is traded off against a high thermal performance. Proceedings of the Royal Society B, 289(1972), 20212414 (2022).

Rezende, EL, Bozinovic, F, Szilágyi, A, Santos, M. Predicting temperature mortality and selection in natural Drosophila populations. Science, 369(6508), 1242-1245  (2020).

Evolutionary responses of energy metabolism, development, and reproduction to artificial selection for increasing heat tolerance in Drosophila subobscuraAndres Mesas, Luis E. Castaneda<p>Adaptations to warming conditions exhibited by ectotherms include increasing heat tolerance but also metabolic changes to reduce maintenance costs (metabolic depression), which can allow them to redistribute the energy surplus to biological fun...Adaptation, Evolutionary Ecology, Experimental Evolution, Life HistoryInês Fragata2022-02-08 01:05:50 View
13 Jan 2019
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Why cooperation is not running away

A nice twist on partner choice theory

Recommended by based on reviews by 2 anonymous reviewers

In this paper, Geoffroy et al. [1] deal with partner choice as a mechanism of maintaining cooperation, and argues that rather than being unequivocally a force towards improved payoffs to everyone through cooperation, partner choice can lead to “over-cooperation” where individuals can evolve to invest so much in cooperation that the costs of cooperating partially or fully negate the benefits from it. This happens when partner choice is consequential and effective, i.e., when interactions are long (so each decision to accept or reject a partner is a bigger stake) and when meeting new partners is frequent when unpaired (so that when one leaves an interaction one can find a new partner quickly). Geoffroy et al. [1] show that this tendency to select for overcooperation under such regimes can be counteracted if individuals base their acceptance-rejection of partners not just on the partner cooperativeness, but also on their own. By using tools from matching theory in economics, they show that plastic partner choice generates positive assortment between cooperativeness of the partners, and in the extreme case of perfectly assortative pairings, makes the pair the unit of selection, which selects for maximum total payoff.
This study is a nice contribution to the literature that illustrates potential complexities with partner choice as a mechanism for cooperation, including how the proximate mechanisms of partner choice can significantly alter the evolutionary trajectory of cooperation. Modeling choice as a reaction norm that depends on one’s own traits also adds a layer of realism to partner choice theory.
The authors are also to be commended for the revisions they made through the review process. Earlier versions of the model somewhat overstated the tendency for fixed partner choice strategies to lead to over cooperation, missing some of the important features in previous models, notably McNamara et al. [2] that can counter this tendency. In this version, the authors acknowledge these factors, mainly, mortality during partner choice (which increases the opportunity cost of forgoing a current partner) and also the fact that endogenous distribution of alternative partners (which will tend to be worse than the overall population distribution, because more cooperative types spend more time attached and less cooperative types more time unattached). These two factors can constrain cooperation from “running away” as the authors put it, but the main point of Geoffroy et al. [1] that plastic choice can create selection against inefficient cooperation stands.
I think the paper will be very stimulating to theoretical and empirical researchers working on partner choice and social behaviors, and happy to recommend it.


[1] Geoffroy, F., Baumard, N., & Andre, J.-B. (2019). Why cooperation is not running away. bioRxiv, ver. 5 peer-reviewed and recommended by PCI Evol Biol. doi: 10.1101/316117
[2] McNamara, J. M., Barta, Z., Fromhage, L., & Houston, A. I. (2008). The coevolution of choosiness and cooperation. Nature, 451, 189–192. doi: 10.1038/nature06455

Why cooperation is not running awayFélix Geoffroy, Nicolas Baumard, Jean-Baptiste André<p>A growing number of experimental and theoretical studies show the importance of partner choice as a mechanism to promote the evolution of cooperation, especially in humans. In this paper, we focus on the question of the precise quantitative lev...Behavior & Social Evolution, Evolutionary TheoryErol Akcay2018-05-15 10:32:51 View