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11 Sep 2017
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Less effective selection leads to larger genomes

Colonisation of subterranean ecosystems leads to larger genome in waterlouse (Aselloidea)

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The total amount of DNA utilized to store hereditary information varies immensely among eukaryotic organisms. Single copy genome sizes – disregarding differences due to ploidy - differ by more than three orders of magnitude ranging from a few million nucleotides (Mb) to hundreds of billions (Gb). With the ever-increasing availability of fully sequenced genomes we now know that most of the difference is due either to whole genome duplication or to variation in the abundance of repetitive elements. Regarding repetitive elements, the evolutionary forces underlying the large variation 'allowing' more or less elements in a genome remain largely elusive. A tentative correlation between an organism's complexity (however this may be adequately measured) and genome size, the so called C-value paradox [1], has long been dismissed. Studies testing for selection on secondary phenotypic effects associated with genome size (cell size, metabolic rates, nutrient availability) have yielded mixed results. Nonadaptive theories capitalizing on a role of deleterious insertion-deletion mutations and genetic drift as the main drivers have likewise received mixed support [2-3]. Overall, most evidence was derived from analyses across broad taxonomical scales [4-6].

Lefébure and colleagues [7] take a different approach. They confine their considerations to a homogeneous, restricted taxonomical group, isopod crustaceans of the superfamily Aselloidea. This taxonomic focus allows the authors to circumvent many of the confounding factors such as phylogenetic inertia, life history divergence and mutation rate variation that tend to trouble analyses across broad taxonomic timescales. Another important feature of the chosen system is the evolutionary independent transition of habitat use that has occurred at least 11 times. One group of species inhabits subterranean ecosystems (groundwater), another group thrives on surface water. Populations of the former live in low-energy habitats and are expected to be outnumbered by their surface dwelling relatives. Interestingly – and a precondition for the study - the groundwater species have significantly larger genomes (up to 137%). With this unique set-up, the authors are able to investigate the link between genome size and evolutionary forces related to a proxy of long-term population size by removing many of the confounding factors a priori.

Upfront, we learn that the dN/dS ratio is higher in the groundwater species. This may either suggest prevalent positive selection or lower efficacy of purifying selection (relaxed constraint) in the group of species in which population sizes are expected to be low. Using a series of population genetic analyses the authors provide compelling evidence for the latter. Analyses are carefully conducted and include models for estimating the intensity and frequency of purifying and positive selection, the DoS (direction of selection) and α statistic. Next the authors also exclude the possibility that increased dN/dS of the subterranean groundwater species may be due to nonfunctionalization, which may result from the subterranean lifestyle.

Overall, these analyses suggest relaxed constraint in smaller populations as the most plausible alternative to explain increased dN/dS ratios. In addition to the efficacy of selection, the authors estimate the timing of the ecological transition under the rationale that the amount of time a species may have been exposed to the subterranean habitat may reflect long term population sizes. To calibrate the 'colonization clock' they apply a neat trick based on the degree of degeneration of the opsin gene (as vision tends to get lost in these habitats). When finally testing which parameters may explain differences in genome size all factors – ecological status, selection efficiency as measured by dN/dS and colonization time - turned out to be significant predictors. Direct estimates of the short term effective population size Ne from polymorphism data, however, did not correlate with genome size. Ruling out the effect of other co-variates such as body size and growth rate the authors conclude that genome size was overall best predicted by long-term population size change upon habitat shift. In that the authors provide convincing evidence that the increase in genome size is linked to a decrease in long-term reduction of selection efficiency of subterranean species. Assuming a bias for insertion mutations over deletion mutations (which is usually the case in eukaryotes) this result is in agreement with the theory of mutational hazard [4-6]. This theory proposed by Michael Lynch postulates that the accumulation of non-functional DNA has a weak deleterious effect that can only be efficiently opposed by natural selection in species with high Ne.

In conclusion, Lefébure and colleagues provide novel and welcome evidence supporting a 'neutralist' hypothesis of genome size evolution without the need to invoke an adaptive component. Methodologically, the study cautions against the common use of polymorphism-based estimates of Ne which are often obfuscated by transitory demographic change. Instead, alternative measures of selection efficacy linked to long-term population size may serve as better predictors of genome size. We hope that this study will stimulate additional work testing the link between Ne and genome size variation in other taxonomical groups [8-9]. Using genome sequences instead of the transcriptome approach applied here may concomitantly further our understanding of the molecular mechanisms underlying genome size change.

References

[1] Thomas, CA Jr. 1971. The genetic organization of chromosomes. Annual Review of Genetics 5: 237–256. doi: 10.1146/annurev.ge.05.120171.001321

[2] Ågren JA, Greiner S, Johnson MTJ, Wright SI. 2015. No evidence that sex and transposable elements drive genome size variation in evening primroses. Evolution 69: 1053–1062. doi: 10.1111/evo.12627

[3] Bast J, Schaefer I, Schwander T, Maraun M, Scheu S, Kraaijeveld K. 2016. No accumulation of transposable elements in asexual arthropods. Molecular Biology and Evolution 33: 697–706. doi: 10.1093/molbev/msv261

[4] Lynch M. 2007. The Origins of Genome Architecture. Sinauer Associates.

[5] Lynch M, Bobay LM, Catania F, Gout JF, Rho M. 2011. The repatterning of eukaryotic genomes by random genetic drift. Annual Review of Genomics and Human Genetics 12: 347–366. doi: 10.1146/annurev-genom-082410-101412

[6] Lynch M, Conery JS. 2003. The origins of genome complexity. Science 302: 1401–1404. doi: 10.1126/science.1089370

[7] Lefébure T, Morvan C, Malard F, François C, Konecny-Dupré L, Guéguen L, Weiss-Gayet M, Seguin-Orlando A, Ermini L, Der Sarkissian C, Charrier NP, Eme D, Mermillod-Blondin F, Duret L, Vieira C, Orlando L, and Douady CJ. 2017. Less effective selection leads to larger genomes. Genome Research 27: 1016-1028. doi: 10.1101/gr.212589.116

[8] Lower SS, Johnston JS, Stanger-Hall KF, Hjelmen CE, Hanrahan SJ, Korunes K, Hall D. 2017. Genome size in North American fireflies: Substantial variation likely driven by neutral processes. Genome Biolology and Evolution 9: 1499–1512. doi: 10.1093/gbe/evx097

[9] Sessegolo C, Burlet N, Haudry A. 2016. Strong phylogenetic inertia on genome size and transposable element content among 26 species of flies. Biology Letters 12: 20160407. doi: 10.1098/rsbl.2016.0407

Less effective selection leads to larger genomesTristan Lefébure, Claire Morvan, Florian Malard, Clémentine François, Lara Konecny-Dupré, Laurent Guéguen, Michèle Weiss-Gayet, Andaine Seguin-Orlando, Luca Ermini, Clio Der Sarkissian, N. Pierre Charrier, David Eme, Florian Mermillod-Blondin, Lau...The evolutionary origin of the striking genome size variations found in eukaryotes remains enigmatic. The effective size of populations, by controlling selection efficacy, is expected to be a key parameter underlying genome size evolution. However...Evolutionary Theory, Genome Evolution, Molecular Evolution, Population Genetics / GenomicsBenoit Nabholz2017-09-08 09:39:23 View
19 Feb 2018
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Genomic imprinting mediates dosage compensation in a young plant XY system

Dosage compensation by upregulation of maternal X alleles in both males and females in young plant sex chromosomes

Recommended by and based on reviews by 3 anonymous reviewers

Sex chromosomes evolve as recombination is suppressed between the X and Y chromosomes. The loss of recombination on the sex-limited chromosome (the Y in mammals) leads to degeneration of both gene expression and gene content for many genes [1]. Loss of gene expression or content from the Y chromosome leads to differences in gene dose between males and females for X-linked genes. Because expression levels are often correlated with gene dose [2], these hemizygous genes have a lower expression levels in the heterogametic sex. This in turn disrupts the stoichiometric balance among genes in protein complexes that have components on both the sex chromosomes and autosomes [3], which could have serious deleterious consequences for the heterogametic sex.
To overcome these deleterious effects of degeneration, the expression levels of dosage sensitive X-linked genes, and in some organisms, entire X chromosomes, are compensated, the expression of the single copy of in the heterogametic sex being increased. Dosage compensation for such genes has evolved in several species, restoring similar expression levels as in the ancestral state in males and/or equal gene expression in males and females [4-8]. The mechanisms for dosage compensation are variable among species and their evolutionary paths are not fully understood, as the few model sex chromosomes studied so far have old, and highly degenerate sex chromosomes [4-7].
Muyle et al. [9] studied the young sex chromosomes of the plant Silene latifolia, which has young sex chromosomes (4 MY) and highly variable dosage compensation [10, 11]. The authors used both an outgroup species without sex chromosomes for obtaining a proxy for ancestral expression levels before Y degeneration, and implemented methods to identify sex-linked genes and disentangle paternal versus maternal allele expression [12]. Using these elements, Muyle et al. [9] reveal upregulation of maternal X alleles in both males and females in the young S. latifolia sex chromosomes [9], possibly by genomic imprinting. The upregulation in both sexes of the maternal X alleles likely yields non-optimal gene expression in females, which is strikingly consistent with the theoretical first step of dosage compensation as postulated by Ohno [8], which predicts restoration of ancestral expression in males, over-expression in females, and unequal expression in the two sexes. These findings provide surprising insight into the earliest stages of dosage compensation, one of the most intriguing aspects of evolutionary biology.

References
[1] Bachtrog D. 2013. Y chromosome evolution: emerging insights into processes of Y-chromosome degeneration? Nature Reviews Genetics 14: 113–124. doi: 10.1038/nrg3366
[2] Malone JH, Cho D-Y, Mattiuzzo NR, Artieri CG, Jiang L, Dale RK, Smith HE, McDaniel J, Munro S, Salit M, Andrews J, Przytycka TM and Oliver B. 2012. Mediation of Drosophila autosomal dosage effects and compensation by network interactions. Genome Biology 13: R28. doi: 10.1186/gb-2012-13-4-r28
[3] Pessia E, Makino T, Bailly-Bechet M, McLysaght A and Marais GAB. 2012. Mammalian X chromosome inactivation evolved as a dosage-compensation mechanism for dosage-sensitive genes on the X chromosome. Proceedings of the National Academy of Sciences of the United States of America. 109: 5346–5351. doi: 10.1073/pnas.1116763109.
[4] Graves JAM. 2016. Evolution of vertebrate sex chromosomes and dosage compensation. Nature Reviews Genetics 17: 33–46. doi: 10.1038/nrg.2015.2
[5] Mank JE. 2013. Sex chromosome dosage compensation: definitely not for everyone. Trends in Genetics 12: 677–683. doi: 10.1016/j.tig.2013.07.005
[6] Pessia E and Engelstädter J. 2014. The evolution of X chromosome inactivation in mammals: the demise of Ohno’s hypothesis? Cellular and Molecular Life Sciences 71: 1383–1394. doi: 10.1007/s00018-013-1499-6
[7] Muyle A, Shearn R and Marais GAB. 2017. The evolution of sex chromosomes and dosage compensation in plants. Genome Biology and Evolution 9: 627–645. doi: 10.1093/gbe/evw282
[8] Ohno S. 1967. Sex chromosomes and sex linked genes. Springer, Berlin Heidelberg New York.
[9] Muyle A, Zemp N, Fruchard C, Cegan R, Vrana J, Deschamps C, Tavares R, Picard F, Hobza R, Widmer A and Marais GAB. 2018. Genomic imprinting mediates dosage compensation in a young plant XY system. bioRxiv 118695, ver. 6 peer-reviewed by Peer Community In Evolutionary Biology. doi: 10.1101/179044
[10] Papadopulos AST, Chester M, Ridout K and Filatov DA. 2015. Rapid Y degeneration and dosage compensation in plant sex chromosomes. Proceedings of the National Academy of Sciences of the United States of America 112: 13021–13026. doi: 10.1073/pnas.1508454112
[11] Bergero R, Qiu S and Charlesworth D. 2015. Gene loss from a plant sex chromosome system. Current Biology 25: 1234–1240. doi: 10.1016/j.cub.2015.03.015
[12] Muyle A, Kafer J, Zemp N, Mousset S, Picard F and Marais GAB. 2016. SEX-DETector: a probabilistic approach to study sex chromosomes in non-model organisms. Genome Biology and Evolution 8: 2530–2543. doi: 10.1093/gbe/evw172

Genomic imprinting mediates dosage compensation in a young plant XY systemAline Muyle, Niklaus Zemp, Cecile Fruchard, Radim Cegan, Jan Vrana, Clothilde Deschamps, Raquel Tavares, Franck Picard, Roman Hobza, Alex Widmer, Gabriel Marais<p>During the evolution of sex chromosomes, the Y degenerates and its expression gets reduced relative to the X and autosomes. Various dosage compensation mechanisms that recover ancestral expression levels in males have been described in animals....Bioinformatics & Computational Biology, Expression Studies, Genome Evolution, Molecular Evolution, Reproduction and SexTatiana Giraud2017-09-20 20:39:46 View
19 Mar 2018
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Natural selection on plasticity of thermal traits in a highly seasonal environment

Is thermal plasticity itself shaped by natural selection? An assessment with desert frogs

Recommended by based on reviews by Dries Bonte, Wolf Blanckenhorn and Nadia Aubin-Horth

It is well known that climatic factors – most notably temperature, season length, insolation and humidity – shape the thermal niche of organisms on earth through the action of natural selection. But how is this achieved precisely? Much of thermal tolerance is actually mediated by phenotypic plasticity (as opposed to genetic adaptation). A prominent expectation is that environments with greater (daily and/or annual) thermal variability select for greater plasticity, i.e. better acclimation capacity. Thus, plasticity might be selected per se.

A Chilean group around Leonardo Bacigalupe assessed natural selection in the wild in one marginal (and extreme) population of the four-eyed frog Pleurodema thaul (Anura: Leptodactylidae) in an isolated oasis in the Atacama Desert, permitting estimation of mortality without much potential of confounding it with migration [1]. Several thermal traits were considered: CTmax – the critical maximal temperature; CTmin – the critical minimum temperature; Tpref – preferred temperature; Q10 – thermal sensitivity of metabolism; and body mass. Animals were captured in the wild and subsequently assessed for thermal traits in the laboratory at two acclimation temperatures (10° & 20°C), defining the plasticity in all traits as the difference between the traits at the two acclimation temperatures. Thereafter the animals were released again in their natural habitat and their survival was monitored over the subsequent 1.5 years, covering two breeding seasons, to estimate viability selection in the wild. The authors found and conclude that, aside from larger body size increasing survival (an unsurprising result), plasticity does not seem to be systematically selected directly, while some of the individual traits show weak signs of selection.

Despite limited sample size (ca. 80 frogs) investigated in only one marginal but very seasonal population, this study is interesting because selection on plasticity in physiological thermal traits, as opposed to selection on the thermal traits themselves, is rarely investigated. The study thus also addressed the old but important question of whether plasticity (i.e. CTmax-CTmin) is a trait by itself or an epiphenomenon defined by the actual traits (CTmax and CTmin) [2-5]. Given negative results, the main question could not be ultimately solved here, so more similar studies should be performed.

References

[1] Bacigalupe LD, Gaitan-Espitia, JD, Barria AM, Gonzalez-Mendez A, Ruiz-Aravena M, Trinder M & Sinervo B. 2018. Natural selection on plasticity of thermal traits in a highly seasonal environment. bioRxiv 191825, ver. 5 peer-reviewed by Peer Community In Evolutionary Biology. doi: 10.1101/191825
[2] Scheiner SM. 1993. Genetics and evolution of phenotypic plasticity. Annual Review in Ecology and Systematics 24: 35–68. doi: 10.1146/annurev.es.24.110193.000343
[3] Scheiner SM. 1993. Plasticity as a selectable trait: Reply to Via. The American Naturalist. 142: 371–373. doi: 10.1086/285544
[4] Via S. 1993. Adaptive phenotypic plasticity - Target or by-product of selection in a variable environment? The American Naturalist. 142: 352–365. doi: 10.1086/285542
[5] Via S. 1993. Regulatory genes and reaction norms. The American Naturalist. 142: 374–378. doi: 10.1086/285542

Natural selection on plasticity of thermal traits in a highly seasonal environmentLeonardo Bacigalupe, Juan Diego Gaitan-Espitia, Aura M Barria, Avia Gonzalez-Mendez, Manuel Ruiz-Aravena, Mark Trinder, Barry Sinervo<p>For ectothermic species with broad geographical distributions, latitudinal/altitudinal variation in environmental temperatures (averages and extremes) are expected to shape the evolution of physiological tolerances and the acclimation capacity ...Adaptation, Evolutionary Ecology, Phenotypic PlasticityWolf Blanckenhorn2017-09-22 23:17:40 View
09 Feb 2018
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Phylodynamic assessment of intervention strategies for the West African Ebola virus outbreak

Simulating the effect of public health interventions using dated virus sequences and geographical data

Recommended by ORCID_LOGO based on reviews by Christian Althaus, Chris Wymant and 1 anonymous reviewer

Perhaps because of its deadliness, the 2013-2016 Ebola Virus (EBOV) epidemics in West-Africa has led to unprecedented publication and sharing of full virus genome sequences. This was both rapid (90 full genomes were shared within weeks [1]) and important (more than 1500 full genomes have been released overall [2]). Furthermore, the availability of the metadata (especially GPS location) has led to depth analyses of the geographical spread of the epidemics [3].
In their work, Dellicour et al. [4] pursue earlier phylogeographical investigations in an original and yet simple approach to address questions of key public health importance. The originality of the approach is dual. First, from a technical standpoint, they capture the spread of infectious diseases in a continuous framework using a novel model that allows for rare long-distance dispersal events. Second, in a more classical discrete meta-population framework, they simulate the effect of public health interventions by pruning the phylogenetic tree and assessing how this affects key parameters. For instance, to simulate the effect of closing borders they remove subsets of the phylogeny that involved dispersal between countries and to simulate the effect of protecting a region by quarantine they remove all the leaves (i.e. the infections sampled) from this region. This phylogeny pruning is both original and simple. It is however limited because it currently assumes that policies are 100% effective and earlier modelling work on human influenza showed that long distance travel bans had to be implemented with >99% efficiency in order to slow epidemic growth from a time scale of days to weeks [5].
From a biological standpoint, Dellicour et al. [4] corroborate earlier findings that highly populated locations (>1,000,000 inhabitants) were crucial in explaining the magnitude of the epidemics but also show the importance of the transmission between the three capital cities. They also show that rare long-distance dispersing events of the virus are not key to explaining the magnitude of the epidemics (even though they assume 100% efficiency of suppressing long-distance event). Finally, thanks to their continuous model they estimate the speed of spread of the epidemics and are able to detect the effect of border closing on this speed.
Overall, this study [4], which involves state-of-the-art Bayesian inference methods of infection phylogenies using MCMC, stands out because of its effort to simulate public health interventions. It stands as an encouragement for the development of intervention models with increased realism and for even faster and larger virus sequence data sharing.

References

[1] Gire et al. 2014. Genomic surveillance elucidates Ebola virus origin and transmission during the 2014 outbreak. Science 345: 1369–1372. doi: 10.1126/science.1259657.
[2] Holmes EC, Dudas G, Rambaut A and Andersen KG. 2016. The evolution of Ebola virus: insights from the 2013-2016 epidemic. Nature 538: 193–200. doi: 10.1038/nature19790.
[3] Dudas et al. 2017. Virus genomes reveal factors that spread and sustained the Ebola epidemic. Nature 544: 309–315 (2017). doi: 10.1038/nature22040.
[4] Dellicour S, Baele G, Dudas G, Faria NR, Pybus OG, Suchard MA, Rambaud A and Lemey P. 2018. Phylodynamic assessment of intervention strategies for the West African Ebola virus outbreak. bioRxiv, 163691, ver. 3 peer-reviewed by Peer Community In Evolutionary Biology. doi: 10.1101/163691.
[5] Hollingsworth TD, Ferguson NM and Anderson RM. 2006. Will travel restrictions control the international spread of pandemic influenza? Nature Medicine 12, 497–499. doi: 10.1038/nm0506-497.

Phylodynamic assessment of intervention strategies for the West African Ebola virus outbreakSimon Dellicour, Guy Baele, Gytis Dudas, Nuno R. Faria, Oliver G. Pybus, Marc A. Suchard, Andrew Rambaut, Philippe Lemey<p>This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (https://doi.org/10.24072/pci.evolbiol.100046). The recent Ebola virus (EBOV) outbreak in West Africa witnessed considerable efforts to obtain viral genom...Phylogenetics / Phylogenomics, Phylogeography & BiogeographySamuel Alizon2017-09-30 13:49:57 View
18 May 2018
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Modularity of genes involved in local adaptation to climate despite physical linkage

Differential effect of genes in diverse environments, their role in local adaptation and the interference between genes that are physically linked

Recommended by based on reviews by Tanja Pyhäjärvi and 1 anonymous reviewer

The genome of eukaryotic species is a complex structure that experience many different interactions within itself and with the surrounding environment. The genetic architecture of a phenotype (that is, the set of genetic elements affecting a trait of the organism) plays a fundamental role in understanding the adaptation process of a species to, for example, different climate environments, or to its interaction with other species. Thus, it is fundamental to study the different aspects of the genetic architecture of the species and its relationship with its surronding environment. Aspects such as modularity (the number of genetic units and the degree to which each unit is affecting a trait of the organism), pleiotropy (the number of different effects that a genetic unit can have on an organism) or linkage (the degree of association between the different genetic units) are essential to understand the genetic architecture and to interpret the effects of selection on the genome. Indeed, the knowledge of the different aspects of the genetic architecture could clarify whether genes are affected by multiple aspects of the environment or, on the contrary, are affected by only specific aspects [1,2].

The work performed by Lotterhos et al. [3] sought to understand the genetic architecture of the adaptation to different environments in lodgepole pine (Pinus contorta), considering as candidate SNPs those previously detected as a result of its extreme association patterns to different environmental variables or to extreme population differentiation. This consideration is very important because the study is only relevant if the studied markers are under the effect of selection. Otherwise, the genetic architecture of the adaptation to different environments would be masked by other (neutral) kind of associations that would be difficult to interpret [4,5]. In order to understand the relationship between genetic architecture and adaptation, it is relevant to detect the association networks of the candidate SNPs with climate variables (a way to measure modularity) and if these SNPs (and loci) are affected by single or multiple environments (a way to measure pleiotropy).

The authors used co-association networks, an innovative approach in this field, to analyse the interaction between the environmental information and the genetic polymorphism of each individual. This methodology is more appropriate than other multivariate methods - such as analysis based on principal components - because it is possible to cluster SNPs based on associations with similar environmental variables. In this sense, the co-association networks allowed to both study the genetic and physical linkage between different co-associations modules but also to compare two different models of evolution: a Modular environmental response architecture (specific genes are affected by specific aspects of the environment) or a Universal pleiotropic environmental response architecture (all genes are affected by all aspects of the environment). The representation of different correlations between allelic frequency and environmental factors (named galaxy biplots) are especially informative to understand the effect of the different clusters on specific aspects of the environment (for example, the co-association network ‘Aridity’ shows strong associations with hot/wet versus cold/dry environments).

The analysis performed by Lotterhos et al. [3], although it has some unavoidable limitations (e.g., only extreme candidate SNPs are selected, limiting the results to the stronger effects; the genetic and physical map is incomplete in this species), includes relevant results and also implements new methodologies in the field. To highlight some of them: the preponderance of a Modular environmental response architecture (evolution in separated modules), the detection of physical linkage among SNPs that are co-associated with different aspects of the environment (which was unexpected a priori), the implementation of co-association networks and galaxy biplots to see the effect of modularity and pleiotropy on different aspects of environment. Finally, this work contains remarkable introductory Figures and Tables explaining unambiguously the main concepts [6] included in this study. This work can be treated as a starting point for many other future studies in the field.

References

[1] Hancock AM, Brachi B, Faure N, Horton MW, Jarymowycz LB, Sperone FG, Toomajian C, Roux F & Bergelson J. 2011. Adaptation to climate across the Arabidopsis thaliana genome. Science 334: 83–86. doi: 10.1126/science.1209244
[2] Wagner GP & Zhang J. The pleiotropic structure of the genotype­phenotype map: the evolvability of complex organisms. Nature Review Genetics 12: 204–213. doi: 10.1038/nrg2949
[3] Lotterhos KE, Yeaman S, Degner J, Aitken S, Hodgins K. 2018. Modularity of genes involved in local adaptation to climate despite physical linkage. bioRxiv 202481, ver. 4 peer-reviewed by Peer Community In Evolutionary Biology. doi: 10.1101/202481
[4] Lotterhos KE & Whitlock MC. 2014. Evaluation of demographic history and neutral parameterization on the performance of FST outlier tests. Molecular Ecology 23: 2178–2192. doi: 10.1111/mec.12725
[5] Lotterhos KE & Whitlock MC. 2015. The relative power of genome scans to detect local adaptation depends on sampling design and statistical method. Molecular Ecology 24: 1031–1046. doi: 10.1111/mec.13100
[6] Paaby AB & Rockman MV. 2013. The many faces of pleiotropy. Trends in Genetics 29: 66-73. doi: 10.1016/j.tig.2012.10.010

Modularity of genes involved in local adaptation to climate despite physical linkageKatie E. Lotterhos, Sam Yeaman, Jon Degner, Sally Aitken, Kathryn Hodgins<p>Background: Physical linkage among genes shaped by different sources of selection is a fundamental aspect of genetic architecture. Theory predicts that evolution in complex environments selects for modular genetic architectures and high recombi...Adaptation, Bioinformatics & Computational Biology, Genome EvolutionSebastian Ernesto Ramos-Onsins2017-10-15 19:21:57 View
05 Jun 2018
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The dynamics of preferential host switching: host phylogeny as a key predictor of parasite prevalence and distribution

Shift or stick? Untangling the signatures of biased host switching, and host-parasite co-speciation

Recommended by based on reviews by Damien de Vienne and Nathan Medd

Many emerging diseases arise by parasites switching to new host species, while other parasites seem to remain with same host lineage for very long periods of time, even over timescales where an ancestral host species splits into two or more new species. The ability to understand these dynamics would form an important part of our understanding of infectious disease.

Experiments are clearly important for understanding these processes, but so are comparative studies, investigating the variation that we find in nature. Such comparative data do show strong signs of non-randomness, and this suggests that the epidemiological and ecological processes might be predictable, at least in part. For example, when we map patterns of parasite presence/absence onto host phylogenies, we often find that certain host clades harbour many more parasites than expected, or that closely-related hosts harbour closely-related parasites. Nevertheless, it remains difficult to interpret these patterns to make inferences about ecological and epidemiological processes. This is partly because non-random associations can arise in multiple ways. For example, parasites might be inherited from the common ancestor of related hosts, or might switch to new hosts, but preferentially establish on novel hosts that are closely related to their existing host. Infection might also influence the shape of host phylogeny, either by increasing the rate of host extinction or, conversely, increasing the rate of speciation (as with manipulative symbionts that might induce reproductive isolation).

These various processes have, by and large, been studied in isolation, but the model introduced by Engelstädter and Fortuna [1], makes an important first step towards studying them together. Without such combined analyses, we will not be able to tell if the processes have their own unique signatures, or whether the same sort of non-randomness can arise in multiple ways.

A major finding of the work is that the size of a host clade can be an important determinant of its overall infection level. This had been shown in previous work, assuming that the host phylogeny was fixed, but the current paper shows that it extends also to situations where host extinction and speciation takes place at a comparable rate to host shifting. This finding, then, calls into question the natural assumption that a clade of host species that is highly parasite ridden, must have some genetic or ecological characteristic that makes them particularly prone to infection, arguing that the clade size, rather than any characteristic of the clade members, might be the important factor. It will be interesting to see whether this prediction about clade size is borne out with comparative studies.

Another feature of the study is that the framework is naturally extendable, to include further processes, such as the influence of parasite presence on extinction or speciation rates. No doubt extensions of this kind will form the basis of important future work.

References

[1] Engelstädter J and Fortuna NZ. 2018. The dynamics of preferential host switching: host phylogeny as a key predictor of parasite prevalence and distribution. bioRxiv 209254 ver. 5 peer-reviewed by Peer Community In Evolutionary Biology. doi: 10.1101/209254

The dynamics of preferential host switching: host phylogeny as a key predictor of parasite prevalence and distributionJan Engelstaedter & Nicole Fortuna<p>New parasites commonly arise through host-shifts, where parasites from one host species jump to and become established in a new host species. There is much evidence that the probability of host-shifts decreases with increasing phylogenetic dist...Bioinformatics & Computational Biology, Evolutionary Epidemiology, Evolutionary Theory, Macroevolution, Phylogenetics / Phylogenomics, Species interactionsLucy Weinert2017-10-30 02:06:06 View
06 Jul 2018
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Variation in competitive ability with mating system, ploidy and range expansion in four Capsella species

When ecology meets genetics: Towards an integrated understanding of mating system transitions and diversity

Recommended by and based on reviews by Yaniv Brandvain, Henrique Teotonio and 1 anonymous reviewer

In the 19th century, C. Darwin and F. Delpino engaged in a debate about the success of species with different reproduction modes, with the later favouring the idea that monoecious plants capable of autonomous selfing could spread more easily than dioecious plants (or self-incompatible hermaphroditic plants) if cross-pollination opportunities were limited [1]. Since then, debate has never faded about how natural selection is responsible for transitions to selfing and can explain the diversity and distribution of reproduction modes we observe in the natural world [2, 3].
Explanations for mating systems diversity, and transitions to selfing in particular, generally fall into two categories: either genetic or ecological. On the genetic side, many theoretical works showed a critical role for mutation load and inbreeding depression, transmission advantage and reproductive assurance in the evolution of selfing, e.g. [4]. Many experimental works were conducted to test theoretical hypotheses and predictions, especially regarding the magnitude of inbreeding depression; see [5] for a review. Ecologically, the presence of selfing populations is usually correlated with fragmented and harsh habitats, on the periphery of ancestral outcrossing populations. The cause of this distribution could be that selfers are better dispersers and colonizers than outcrossers, or variations in other life-history traits [6]. Yet, few experiments were run to assess whether selfing species or populations have effectively different ecological characteristics, and even scarcer are experiments evaluating both the roles of mutational load and life-history traits evolution. This is the aim of the present study by X. Yang et al [7].
The study of Yang et al [7], together with that of Petrone Mendoza et al. [8], supervised by S. Glémin and M. Lascoux, is probably one of the first to conduct experiments where the competitive abilities are compared between and within species. Using 4 species of the Capsella genus, annual plants from the mustard family, they tested the theoretical predictions that i) the transition from outcrossing to selfing resulted in reduced competitive ability at higher densities, because of the accumulation of deleterious mutations and/or the evolution of life-history traits in an open habitat and a colonization/dispersal trade-off; ii) that reduced competitive ability of selfers should be less pronounced in polyploid then diploid species because the effect of partially recessive deleterious mutations would be buffered; and iii) that competitive ability of selfers should decline with historical range expansion because of the expansion load [9].
Of the 4 Capsella species studied, only one of them, presumably the ancestral, is a diploid outcrosser with a small distribution but large population sizes. The three other species are selfers, two diploids with independent histories of transitions from outcrossing, and another, tetraploid, resulting from a recent hybridization between one of the diploid selfer and the diploid outcrossing ancestor. Many accessions from each species were sampled and individuals assayed for their competitive ability against a tester species or alone, for vegetative and reproductive traits. The measured vegetative traits (rosette surface at two stages, growth rate and flowering probability) showed no differentiation between selfers and outcrossers. To the contrary, reproductive traits (number of flowers) followed theoretical predictions: selfing species are more sensitive to competition than the outcrossing species, with polyploid selfing species being intermediate between the diploid selfers and the diploid outcrosser, and within the tetraploid selfing species (where sampling was quite significant across a large geographical range) sensitivity to competition increased with range expansion.
The study of Yang et al. [7] suffers from several limitations, such that alternative explanations cannot be discarded in the absence of further experimental data. They nonetheless provide the reader with a nice discussion and prospects on how to untwine the causes and the consequences of transitions to selfing. Their study also brings up to date questions about the joint evolution of mating system and life-history traits, which needs a renewed interest from an empirical and theoretical point of view. The results of Yang et al. raise for instance the question of whether it is indeed expected that only reproductive traits, and not vegetative traits, should evolve with the transition to selfing.
The recommandation and evaluation of this paper have been made in collaboration with Thomas Lesaffre.

References

[1] Darwin, C. R. (1876). The effects of cross and self fertilization in the vegetable kingdom. London: Murray. [2] Stebbins, G. L. (1957). Self fertilization and population variability in the higher plants. The American Naturalist, 91, 337-354. doi: 10.1086/281999
[3] Harder, L.D. & Barrett, S. C. H. (2006). Ecology and evolution of flowers. Oxford: Oxford University Press. [4] Porcher, E. & Lande, R. (2005). The evolution of self-fertilization and inbreeding depression under pollen discounting and pollen limitation. Journal of Evolutionary Biology, 18(3), 497-508. doi: 10.1111/j.1420-9101.2005.00905.x
[5] Winn, A.A., et al. (2011). Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interference and stable mixed mating. Evolution, 65(12), 3339-3359. doi: 10.1111/j.1558-5646.2011.01462.x
[6] Munoz, F., Violle, C. & Cheptou, P.-O. (2016). CSR ecological strategies and plant mating systems: outcrossing increases with competitiveness but stress-tolerance is related to mixed mating. Oikos, 125(9), 1296-1303. doi: 10.1111/oik.02328
[7] Yang, X., Lascoux, M. & Glémin, S (2018). Variation in competitive ability with mating system, ploidy and range expansion in four Capsella species. bioRxiv, 214866, ver. 5 recommended and peer-reviewed by PCI Evol Biol. doi: 10.1101/214866
[8] Petrone Mendoza, S., Lascoux, M. & Glémin, S. (2018). Competitive ability of Capsella species with different mating systems and ploidy levels. Annals of Botany 121(6), 1257-1264. doi: 10.1093/aob/mcy014
[9] Peischl, S. & Excoffier, L. (2015). Expansion load: recessive mutations and the role of standing genetic variation. Molecular Ecology, 24(9): 2084-2094. doi: 10.1111/mec.13154

Variation in competitive ability with mating system, ploidy and range expansion in four Capsella speciesXuyue Yang, Martin Lascoux and Sylvain Glémin<p>Self-fertilization is often associated with ecological traits corresponding to the ruderal strategy in Grime’s Competitive-Stress-tolerant-Ruderal (CSR) classification of ecological strategies. Consequently, selfers are expected to be less comp...Evolutionary Ecology, Population Genetics / Genomics, Reproduction and Sex, Species interactionsSylvain Billiard2017-11-06 19:54:52 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

Recommended by and

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.

References

[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: https://doi.org/10.1111/evo.12794

[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: https://doi.org/10.1073/pnas.1320393111

[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: https://doi.org/10.1111/j.1558-5646.2011.01558.x

[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: https://doi.org/10.1093/molbev/mss211

[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: https://doi.org/10.1016/j.cub.2017.08.043

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
28 Mar 2019
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Ancient tropical extinctions contributed to the latitudinal diversity gradient

One (more) step towards a dynamic view of the Latitudinal Diversity Gradient

Recommended by and ORCID_LOGO based on reviews by Juan Arroyo, Joaquín Hortal, Arne Mooers, Joaquin Calatayud and 2 anonymous reviewers

The Latitudinal Diversity Gradient (LDG) has fascinated natural historians, ecologists and evolutionary biologists ever since [1] described it about 200 years ago [2]. Despite such interest, agreement on the origin and nature of this gradient has been elusive. Several tens of hypotheses and models have been put forward as explanations for the LDG [2-3], that can be grouped in ecological, evolutionary and historical explanations [4] (see also [5]). These explanations can be reduced to no less than 26 hypotheses, which account for variations in ecological limits for the establishment of progressively larger assemblages, diversification rates, and time for species accumulation [5]. Besides that, although in general the tropics hold more species, different taxa show different shapes and rates of spatial variation [6], and a considerable number of groups show reverse patterns, with richer assemblages in cold temperate regions (see e.g. [7-9]).
Understanding such complexity needs integrating ecological and evolutionary research into the wide temporal and spatial perspectives provided by the burgeoning field of biogeography. This integrative discipline ¬–that traces back to Humboldt himself (e.g. [10])– seeks to put together historical and functional explanations to explain the complex dynamics of Earth’s biodiversity. Different to quantum physicists, biogeographers cannot pursue the ultimate principle behind the patterns we observe in nature due to the interplay of causes and effects, which in fact tell us that there is not such a single principle. Rather, they need to identify an array of basic principles coming from different perspectives, to then integrate them into models that provide realistic –but never simple– explanations to biodiversity gradients such as LDG (see, e.g., [5; 11]). That is, rather than searching for a sole explanation, research on the LDG must aim to identify as many signals hidden in the pattern as possible, and provide hypotheses or models that account for these signals. To later integrate them and, whenever possible, to validate them with empirical data on the organisms’ distribution, ecology and traits, phylogenies, fossils, etc.
Within this context, Meseguer & Condamine [12] provide a novel perspective to LDG research using phylogenetic and fossil evidence on the origin and extinction of taxa within the turtle, crocodile and lizard (i.e. squamate) lineages. By digging into deep time down to the Triassic (about 250 Myr ago) they are able to identify several episodes of flattening and steepening of the LDG for these three clades. Strikingly, their results show similar diversification rates in the northern hemisphere and in the equator during the over 100 Myr long global greenhouse period that extends from the late Jurassic to the Cretaceous and early Neogene. During this period, the LDG for these three groups would have appeared quite even across a mainly tropical Globe, although the equatorial regions were apparently much more evolutionarily dynamic. The equator shows much higher rates of origination and extinction of branches throughout the Cretaceous, but they counteract each other so net diversification is similar to that of the northern hemisphere in all three groups. The transition to a progressively colder Earth in the Paleogene (starting around 50 Myr ago) provokes a mass extinction in the three clades, which is compensated in the equator by the dispersal of many taxa from the areas that currently pertain to the Holarctic biogeographical realm. Finally, during the coldhouse Earth’s climatic conditions of the Neogene only squamates show significant positive diversification rates in extratropical areas, while the diversity of testudines remains, and crocodiles continue declining progressively towards oblivion in the whole world.
Meseguer & Condamine [12] attribute these temporal patterns to the so-called asymmetric gradient of extinction and dispersal (AGED) framework. Here, the dynamics of extinction-at and dispersal-from high latitudes during colder periods increase the steepness of the LDG. Whereas the gradient flattens when Earth warms up as a result of dispersal from the equator followed by increased diversification in extratropical regions. This idea in itself is not new, for the influence of climatic oscillations on diversification rates is well known, at least for the Pleistocene Ice Ages [13], as is the effect of niche conservatism on the LDG [14]. Nevertheless, Meseguer & Condamine’s AGED provides a synthetic verbal model that could allow integrating the three main types of processes behind the LDG into a single framework. To do this it would be necessary to combine AGED’s cycles of dispersal and diversification with realistic models of: (1) the ecological limits to host rich assemblages in the colder and less productive temperate climatic domains; (2) the variations in diversification rates with shifts in temperature and/or energy regimes; and (3) the geographical patterns of climatic oscillation through time that determine the time for species accumulation in each region.
Integrating these models may allow transposing Meseguer & Condamine’s [12] framework into the more mechanistic macroecological models advocated by Pontarp et al. [5]. This type of mechanistic models has been already used to understand the development of biodiversity gradients through the climatic oscillations of the Pleistocene and the Quaternary (e.g. [11]). So the challenge in this case would be to generate a realistic scenario of geographical dynamics that accounts for plate tectonics and long-term climatic oscillations. This is still a major gap and we would benefit from the integrated work by historical geologists and climatologists here. For instance, there is little doubt about the progressive cooling through the Cenozoic based in isotope recording in sea floor sediments [15]. Meseguer & Condamine [12] use this evidence for separating greenhouse, transition and coldhouse world scenarios, which should not be a problem for these rough classes. However, a detailed study of the evolutionary correlation of true climate variables across the tree of life is still pending, as temperature is inferred only for sea water in an ice-free ocean, say earlier half of the Cenozoic [15]. Precipitation regime is even less known. Such scenario would provide a scaffold upon which the temporal dynamics of several aspects of the generation and loss of biodiversity can be modelled. Additionally, one of the great advantages of selecting key clades to study the LDG would be to determine the functional basis of diversification. There are species traits that are well known to affect speciation and extinction probabilities, such as reproductive strategies or life histories (e.g. [16]). Whereas these traits might also be a somewhat redundant effect of climatic causes, they might foster (i.e. “extended reinforcement”, [17]) or slow diversification. Even so, it is unlikely that such a model would account for all the latitudinal variation in species richness. But it will at least provide a baseline for the main latitudinal variations in the diversity of the regional communities (sensu [18]) worldwide. Within this context the effects of recent ecological, evolutionary and historical processes, such as environmental heterogeneity, current diversification rates or glacial cycles, will only modify the general LDG pattern resulting from the main processes contained in Meseguer & Condamine’s AGED, thereby providing a more comprehensive understanding of the geographical gradients of diversity.

References
[1] Humboldt, A. v. (1808). Ansichten der Natur, mit wissenschaftlichen Erläuterungen. J. G. Cotta, Tübingen.
[2] Hawkins, B. A. (2001). Ecology's oldest pattern? Trends in Ecology & Evolution, 16, 470. doi: 10.1016/S0169-5347(01)02197-8
[3] Lomolino, M. V., Riddle, B. R. & Whittaker, R. J. (2017). Biogeography. Fifth Edition. Sinauer Associates, Inc., Sunderland, Massachussets.
[4] Mittelbach, G. G., Schemske, D. W., Cornell, H. V., Allen, A. P., Brown, J. M., Bush, M. B., Harrison, S. P., Hurlbert, A. H., Knowlton, N., Lessios, H. A., McCain, C. M., McCune, A. R., McDade, L. A., McPeek, M. A., Near, T. J., Price, T. D., Ricklefs, R. E., Roy, K., Sax, D. F., Schluter, D., Sobel, J. M. & Turelli, M. (2007). Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecology Letters, 10, 315-331. doi: 10.1111/j.1461-0248.2007.01020.x
[5] Pontarp, M., Bunnefeld L., Cabral, J. S., Etienne, R. S., Fritz, S. A., Gillespie, R. Graham, C. H., Hagen, O., Hartig, F., Huang, S., Jansson, R., Maliet, O., Münkemüller, T., Pellissier, L., Rangel, T. F., Storch, D., Wiegand, T. & Hurlbert, A. H. (2019). The latitudinal diversity gradient: novel understanding through mechanistic eco-evolutionary models. Trends in ecology & evolution, 34, 211-223. doi: 10.1016/j.tree.2018.11.009
[6] Hillebrand, H. (2004). On the generality of the latitudinal diversity gradient. The American Naturalist, 163, 192-211. doi: 10.1086/381004
[7] Santos, A. M. C. & Quicke, D. L. J. (2011). Large-scale diversity patterns of parasitoid insects. Entomological Science, 14, 371-382. doi: 10.1111/j.1479-8298.2011.00481.x
[8] Morinière, J., Van Dam, M. H., Hawlitschek, O., Bergsten, J., Michat, M. C., Hendrich, L., Ribera, I., Toussaint, E. F. A. & Balke, M. (2016). Phylogenetic niche conservatism explains an inverse latitudinal diversity gradient in freshwater arthropods. Scientific Reports, 6, 26340. doi: 10.1038/srep26340
[9] Weiser, M. D., Swenson, N. G., Enquist, B. J., Michaletz, S. T., Waide, R. B., Zhou, J. & Kaspari, M. (2018). Taxonomic decomposition of the latitudinal gradient in species diversity of North American floras. Journal of Biogeography, 45, 418-428. doi: 10.1111/jbi.13131
[10] Humboldt, A. v. (1805). Essai sur la geographie des plantes; accompagné d'un tableau physique des régions equinoxiales. Levrault, Paris.
[11] Rangel, T. F., Edwards, N. R., Holden, P. B., Diniz-Filho, J. A. F., Gosling, W. D., Coelho, M. T. P., Cassemiro, F. A. S., Rahbek, C. & Colwell, R. K. (2018). Modeling the ecology and evolution of biodiversity: Biogeographical cradles, museums, and graves. Science, 361, eaar5452. doi: 10.1126/science.aar5452
[12] Meseguer, A. S. & Condamine, F. L. (2019). Ancient tropical extinctions contributed to the latitudinal diversity gradient. bioRxiv, 236646, ver. 4 peer-reviewed and recommended by PCI Evol Biol. doi: 10.1101/236646
[13] Jansson, R., & Dynesius, M. (2002). The fate of clades in a world of recurrent climatic change: Milankovitch oscillations and evolution. Annual review of ecology and systematics, 33(1), 741-777. doi: 10.1146/annurev.ecolsys.33.010802.150520
[14] Wiens, J. J., & Donoghue, M. J. (2004). Historical biogeography, ecology and species richness. Trends in ecology & evolution, 19, 639-644. doi: 10.1016/j.tree.2004.09.011
[15] Zachos, J. C., Dickens, G. R., & Zeebe, R. E. (2008). An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics. Nature, 451, 279-283. doi: 10.1038/nature06588
[16] Zúñiga-Vega, J. J., Fuentes-G, J. A., Ossip-Drahos, A. G., & Martins, E. P. (2016). Repeated evolution of viviparity in phrynosomatid lizards constrained interspecific diversification in some life-history traits. Biology letters, 12, 20160653. doi: 10.1098/rsbl.2016.0653
[17] Butlin, R. K., & Smadja, C. M. (2018). Coupling, reinforcement, and speciation. The American Naturalist, 191, 155-172. doi: 10.1086/695136
[18] Ricklefs, R. E. (2015). Intrinsic dynamics of the regional community. Ecology letters, 18, 497-503. doi: 10.1111/ele.12431

Ancient tropical extinctions contributed to the latitudinal diversity gradientAndrea S. Meseguer, Fabien Condamine<p>Biodiversity currently peaks at the equator, decreasing toward the poles. Growing fossil evidence suggest that this hump-shaped latitudinal diversity gradient (LDG) has not been persistent through time, with similar species diversity across lat...Evolutionary Dynamics, Evolutionary Ecology, Macroevolution, Paleontology, Phylogenetics / Phylogenomics, Phylogeography & BiogeographyJoaquín Hortal2017-12-20 14:58:01 View
16 Nov 2018
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Fine-grained habitat-associated genetic connectivity in an admixed population of mussels in the small isolated Kerguelen Islands

Introgression from related species reveals fine-scale structure in an isolated population of mussels and causes patterns of genetic-environment associations

Recommended by based on reviews by Thomas Broquet and Tatiana Giraud

Assessing population connectivity is central to understanding population dynamics, and is therefore of great importance in evolutionary biology and conservation biology. In the marine realm, the apparent absence of physical barriers, large population sizes and high dispersal capacities of most organisms often result in no detectable structure, thereby hindering inferences of population connectivity. In a review paper, Gagnaire et al. [1] propose several ideas to improve detection of population connectivity. Notably, using simulations they show that under certain circumstances introgression from one species into another may reveal cryptic population structure within that second species.
The isolated Kerguelen archipelago in the south of Indian Ocean represents a typical situation where the structure of coastal marine organisms is expected to be difficult to detect. In an elegant genomic study, Fraïsse et al. [2] take advantage of introgression from foreign lineages to infer fine-grained population structure in a population of mussels around the Kerguelen archipelago, and investigate its association with environmental variables. Using a large panel of genome-wide markers (GBS) and applying a range of methods that unravel patterns of divergence and gene flow among lineages, they first find that the Kerguelen population is highly admixed, with a major genetic background corresponding to the southern mussel lineage Mytilus platensis introgressed by three northern lineages. By selecting a panel of loci enriched in ancestry-informative SNPs (ie, SNPs highly differentiated among northern lineages) they then detect a fine-scale genetic structure around the Kerguelen archipelago, and identify a major connectivity break. They further show an associating between the genetic structure and environmental variables, particularly the presence of Macrocystis kelp, a marker of habitat exposure to waves (a feature repeatedly evidenced to be important for mussels). While such association pattern could lead to the interpretation that differentiated SNPs correspond to loci directly under selection or linked with such loci, and even be considered as support for adaptive introgression, Fraïsse et al. [2] convincingly show by performing simulations that the genetic-environment association detected can be entirely explained by dispersal barriers associated with environmental variables (habitat-associated connectivity). They also explain why the association is better detected by ancestry-informative SNPs as predicted by Gagnaire et al. [1]. In addition, intrinsic genetic incompatibilities, which reduce gene flow, tend to become trapped at ecotones due to ecological selection, even when loci causing genetic incompatibilities are unlinked with loci involved in adaption to local ecological conditions (Bierne et al. [3]’s coupling hypothesis), leading to correlations between environmental variables and loci not involved in local adaptation. Notably, in Fraïsse et al. [2]’s study, the association between the kelp and ancestry-informative alleles is not consistent throughout the archipelago, casting further doubt on the implication of these alleles in local adaptation.
The study of Fraïsse et al. [2] is therefore an important contribution to evolutionary biology because 1) it provides an empirical demonstration that alleles of foreign origin can be pivotal to detect fine-scale connectivity patterns and 2) it represents a test case of Bierne et al. [3]’s coupling hypothesis, whereby introgressed alleles also enhance patterns of genetic-environment associations. Since genomic scan or GWAS approaches fail to clearly reveal loci involved in local adaptation, how can we disentangle environment-driven selection from intrinsic reproductive barriers and habitat-associated connectivity? A related question is whether we can reliably identify cases of adaptive introgression, which have increasingly been put forward as a mechanism involved in adaptation [4]. Unfortunately, there is no easy answer, and the safest way to go is to rely – where possible – on independent information [5], in particular functional studies of the detected loci, as is for example the case in the mimetic butterfly Heliconius literature (e. g., [6]) where several loci controlling colour pattern variation are well characterized.

References

[1] Gagnaire, P.-A., Broquet, T., Aurelle, D., Viard, F., Souissi, A., Bonhomme, F., Arnaud-Haond, S., & Bierne, N. (2015). Using neutral, selected, and hitchhiker loci to assess connectivity of marine populations in the genomic era. Evolutionary Applications, 8, 769–786. doi: 10.1111/eva.12288
[2] Fraïsse, C., Haguenauer, A., Gerard, K., Weber, A. A.-T., Bierne, N., & Chenuil, A. (2018). Fine-grained habitat-associated genetic connectivity in an admixed population of mussels in the small isolated Kerguelen Islands. bioRxiv, 239244, ver. 4 peer-reviewed and recommended by PCI Evol Biol. doi: 10.1101/239244
[3] Bierne, N., Welch, J., Loire, E., Bonhomme, F., & David, P. (2011). The coupling hypothesis: why genome scans may fail to map local adaptation genes. Molecular Ecology, 20, 2044–2072. doi: 10.1111/j.1365-294X.2011.05080.x
[4] Hedrick, P. W. (2013). Adaptive introgression in animals: examples and comparison to new mutation and standing variation as sources of adaptive variation. Molecular Ecology, 22, 4606–4618. doi: 10.1111/mec.12415
[5] Ravinet, M., Faria, R., Butlin, R. K., Galindo, J., Bierne, N., Rafajlović, M., Noor, M. A. F., Mehlig, B., & Westram, A. M. (2017). Interpreting the genomic landscape of speciation: a road map for finding barriers to gene flow. Journal of Evolutionary Biology, 30, 1450–1477. doi: 10.1111/jeb.13047.
[6] Jay, P., Whibley, A., Frézal, L., Rodríguez de Cara, M. A., Nowell, R. W., Mallet, J., Dasmahapatra, K. K., & Joron, M. (2018). Supergene evolution triggered by the introgression of a chromosomal inversion. Current Biology, 28, 1839–1845.e3. doi: 10.1016/j.cub.2018.04.072

Fine-grained habitat-associated genetic connectivity in an admixed population of mussels in the small isolated Kerguelen IslandsChristelle Fraïsse, Anne Haguenauer, Karin Gerard, Alexandra Anh-Thu Weber, Nicolas Bierne, Anne Chenuil<p>Reticulated evolution -i.e. secondary introgression / admixture between sister taxa- is increasingly recognized as playing a key role in structuring infra-specific genetic variation and revealing cryptic genetic connectivity patterns. When admi...Hybridization / Introgression, Phylogeography & Biogeography, Population Genetics / GenomicsMarianne Elias2017-12-28 14:16:16 View