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02 May 2023
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Host-symbiont-gene phylogenetic reconciliation

Reconciling molecular evolution and evolutionary ecology studies: a phylogenetic reconciliation method for gene-symbiont-host systems

Recommended by based on reviews by Vincent Berry and Catherine Matias

Interactions between species are a driving force in evolution. Many organisms host symbiotic partners that live all or part of their life in or on their host. Whether they are mutualistic or parasitic, these symbiotic associations impose strong selective pressures on both partners and affect their evolutionary trajectories. In fine, they can have a significant impact on the diversification patterns of both host and symbiont lineages, with symbiotic lineages sometimes speciating simultaneously with their hosts and/or switching from one host species to another. Long-term associations between species can also result in gene transfers between the involved organisms. Those lateral gene transfers are a source of ecological innovation but can obscure the phylogenetic signals and render the process of phylogenetic reconstructions complex (Lerat et al. 2003).

Methods known as reconciliations explore similarities and differences between phylogenetic trees. They have been widely used to both compare the diversification patterns of hosts and symbionts and identify lateral gene transfers between species. Though the reconciliation approaches used in host/ symbiont and species/ gene phylogenetic studies are identical, they are always applied separately to solve either molecular evolution questions or investigate the evolution of ecological interactions. However, the two questions are often intimately linked and the current interest in multi-level systems (e.g. the holobiont concept) calls for a unique model that will take into account three-level nested organization (gene/symbiont/ host) where both symbiont and genes can transfer among hosts. 

Here Menet and collaborators (2023) provide such a model to produce three-level reconciliations. In order to do so, they extend the two-level reconciliation model implemented in “ALE” software (Szöllősi et al. 2013), one of the most used and proven reconciliation methods. Briefly, given a symbiont gene tree, a symbiont tree and a host tree, as in previous reconciliation models, the symbiont tree is mapped onto the host tree by mixing three types of events: Duplication, Transfer or Loss (DTL), with a possibility of the symbiont evolving temporarily outside the host phylogeny (in a “ghost” host lineage). The gene tree evolves similarly inside the symbiont tree, but horizontal transfers are constrained to symbionts co-occurring within the same host. Joint reconciliation scenarios are reconstructed and DTL event rates and likelihoods are estimated according to the model. As a nice addition, the authors propose a method to infer the symbiont phylogeny through amalgamation from gene trees and a host tree.

The authors then explore the diverse possibilities offered by this method by testing it on both simulated datasets and biological datasets in order to check whether considering three nested levels is worthwhile. They convincingly show that three-level reconciliation has a better capacity to retrieve the symbiont donors and receivers of horizontal gene transfers, probably because transfers are constrained by additional elements relevant to the biological systems. Using, aphids, their obligate endosymbionts, and the symbiont genes involved in their nutritional functions, they identify horizontal gene transfers between aphid symbionts that are missed by two-level reconciliations but detected by expertise (Manzano-Marín et al. 2020). The other dataset presented here is on the human pathogen Helicobacter pylori, which history is supposed to reflect human migration. They use more than 1000 H. pylori gene families, and four populations, and use likelihood computations to compare different hypotheses on the diversification of the host.

In summary, this study is a proof-of-concept of a 3-level reconciliation, where the authors manage to convey the applicability of their framework to many biological systems. Reported complexities, confirmed by reported running times, show that the method is computationally efficient. Without a doubt, the tool presented here will be very useful to evolutionary biologists who want to investigate multi-scale cophylogenies and it will move forward the study of associations between host and symbionts when symbiont genomic data are available.

REFERENCES

Lerat, E., Daubin, V., & Moran, N. A. (2003). From gene trees to organismal phylogeny in prokaryotes: the case of the γ-Proteobacteria. PLoS biology, 1(1), e19.
https://doi.org/10.1371/journal.pbio.0000019
 
Manzano-Marın, A., Coeur d'acier, A., Clamens, A. L., Orvain, C., Cruaud, C., Barbe, V., & Jousselin, E. (2020). Serial horizontal transfer of vitamin-biosynthetic genes enables the establishment of new nutritional symbionts in aphids' di-symbiotic systems. The ISME Journal, 14(1), 259-273.
https://doi.org/10.1038/s41396-019-0533-6

Menet H, Trung AN, Daubin V, Tannier E (2023) Host-symbiont-gene phylogenetic reconciliation. bioRxiv, 2022.07.01.498457, ver. 2 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.07.01.498457

Szöllősi, G. J., Rosikiewicz, W., Boussau, B., Tannier, E., & Daubin, V. (2013). Efficient exploration of the space of reconciled gene trees. Systematic biology, 62(6), 901-912.
https://doi.org/10.1093/sysbio/syt054

Host-symbiont-gene phylogenetic reconciliationHugo Menet, Alexia Nguyen Trung, Vincent Daubin, Eric Tannier<p style="text-align: justify;"><strong>Motivation:</strong>&nbsp;Biological systems are made of entities organized at different scales e.g. macro-organisms, symbionts, genes...) which evolve in interaction.<br>These interactions range from indepe...Bioinformatics & Computational Biology, Phylogenetics / PhylogenomicsEmmanuelle Jousselin2022-08-21 18:34:27 View
02 May 2023
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Durable resistance or efficient disease control? Adult Plant Resistance (APR) at the heart of the dilemma

Plant resistance to pathogens: just you wait?

Recommended by based on reviews by Jean-Paul Soularue and 1 anonymous reviewer

In this preprint, Rimbaud et al. (2023) examine whether Adult Plant Resistance (APR), where plants delay their response to pathogens, is a viable alternative when the solution to evolve complete resistance from the seedling stage exists. At first glance, delaying resistance seems like a counter-intuitive strategy, unless it can result in a weaker selection of the pathogen, and therefore slow down its adaption to plant resistance.

The approach of Rimbaud et al. is to incorporate as much of the mechanisms as possible into a model. By accounting for explicit spatio-temporal dynamics, stochasticity, and the coupling between demography and population genetics, to simulate an agricultural landscape, they reach a nuanced conclusion.

Weaker and delayed activation of genes that confer APR does indeed reduce the selection pressure acting on the pathogen, at the cost of overall less effective protection. The alternative strategy of rapid or complete activation of these genes, although it results in better results in defending against the pathogen, is at risk of being overcome because it introduces a stronger selection pressure.

One important feature of this work is that it accounts for agricultural practices. The landscape that is simulated can account for monoculture, mosaic cultures, mixed cultures, and rotations of crops (with different strategies for resistance). This introduces an interesting element to the conclusion: that human practices will have an impact on the selection pressures acting within the system.

Perhaps the most striking result is that, for the plants, it might be more beneficial to bear the cost of a wild-type pathogen that can benefit from delayed activation of resistance, and therefore exclude the more virulent strains by simply being there first, and essentially buying the plant some time before it activates its resistance more completely. When the landscape is aggregated, even wild-type pathogens can cause severe epidemics; increasing fragmentation, because it enables connectivity between patches of plants with different strategies, allows pathogens to move across cultivars, and reduces the epidemic risk on susceptible plants.

These results should encourage scaling up the perspective on APR, and indeed Rimbaud et al. adopt a landscape-scale perspective, to show that APR genes and genes conferring more complete resistance early on can have synergistic effects. This is, again, both an interesting result for evolutionary biologists, but also a useful way to prioritize different crop management strategies over large spatial scales.

References

Rimbaud, Loup, et al. Durable Resistance or Efficient Disease Control? Adult Plant Resistance (APR) at the Heart of the Dilemma. 2023. bioRxiv, ver. 2 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.08.30.505787

Durable resistance or efficient disease control? Adult Plant Resistance (APR) at the heart of the dilemmaLoup Rimbaud, Julien Papaïx, Jean-François Rey, Benoît Moury, Luke G. Barrett, Peter H. Thrall<p style="text-align: justify;">Adult plant resistance (APR) is an incomplete and delayed protection of plants against pathogens. At first glance, such resistance should be less efficient than classical major-effect resistance genes, which confer ...Adaptation, Evolutionary Applications, Evolutionary EpidemiologyTimothée Poisot2022-09-02 16:36:32 View
13 Apr 2023
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The landscape of nucleotide diversity in Drosophila melanogaster is shaped by mutation rate variation

An unusual suspect: the mutation landscape as a determinant of local variation in nucleotide diversity

Recommended by based on reviews by David Castellano and 1 anonymous reviewer

Sometimes, important factors for explaining biological processes fall through the cracks, and it is only through careful modeling that their importance eventually comes out to light. In this study, Barroso and Dutheil introduce a new method based on the sequentially Markovian coalescent (SMC, Marjoran and Wall 2006) for jointly estimating local recombination and coalescent rates along a genome. Unlike previous SMC-based methods, however, their method can also co-estimate local patterns of variation in mutation rates. 

This is a powerful improvement which allows them to tackle questions about the reasons for the extensive variation in nucleotide diversity across the chromosomes of a species - a problem that has plagued the minds of population geneticists for decades (Begun and Aquadro 1992, Andolfatto 2007, McVicker et al., 2009, Pouyet and Gilbert 2021). The authors find that variation in de novo mutation rates appears to be the most important factor in determining nucleotide diversity in Drosophila melanogaster. Though seemingly contradicting previous attempts at addressing this problem (Comeron 2014), they take care to investigate and explain why that might be the case.

Barroso and Dutheil have also taken care to carefully explain the details of their new approach and have carried a very thorough set of analyses comparing competing explanations for patterns of nucleotide variation via causal modeling. The reviewers raised several issues involving choices made by the authors in their analysis of variance partitioning, the proper evaluation of the role of linked selection and the recombination rate estimates emerging from their model. These issues have all been extensively addressed by the authors, and their conclusions seem to remain robust. The study illustrates why the mutation landscape should not be ignored as an important determinant of local variation in genetic diversity, and opens up questions about the generalizability of these results to other organisms.

REFERENCES

Andolfatto, P. (2007). Hitchhiking effects of recurrent beneficial amino acid substitutions in the Drosophila melanogaster genome. Genome research, 17(12), 1755-1762. https://doi.org/10.1101/gr.6691007

Barroso, G. V., & Dutheil, J. Y. (2021). The landscape of nucleotide diversity in Drosophila melanogaster is shaped by mutation rate variation. bioRxiv, 2021.09.16.460667, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2021.09.16.460667

Begun, D. J., & Aquadro, C. F. (1992). Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature, 356(6369), 519-520. https://doi.org/10.1038/356519a0

Comeron, J. M. (2014). Background selection as baseline for nucleotide variation across the Drosophila genome. PLoS Genetics, 10(6), e1004434. https://doi.org/10.1371/journal.pgen.1004434

Marjoram, P., & Wall, J. D. (2006). Fast" coalescent" simulation. BMC genetics, 7, 1-9. https://doi.org/10.1186/1471-2156-7-16

McVicker, G., Gordon, D., Davis, C., & Green, P. (2009). Widespread genomic signatures of natural selection in hominid evolution. PLoS genetics, 5(5), e1000471. https://doi.org/10.1371/journal.pgen.1000471

Pouyet, F., & Gilbert, K. J. (2021). Towards an improved understanding of molecular evolution: the relative roles of selection, drift, and everything in between. Peer Community Journal, 1, e27. https://doi.org/10.24072/pcjournal.16

The landscape of nucleotide diversity in Drosophila melanogaster is shaped by mutation rate variationGustavo V Barroso, Julien Y Dutheil<p style="text-align: justify;">What shapes the distribution of nucleotide diversity along the genome? Attempts to answer this question have sparked debate about the roles of neutral stochastic processes and natural selection in molecular evolutio...Bioinformatics & Computational Biology, Population Genetics / GenomicsFernando Racimo2022-10-30 07:52:07 View
11 Apr 2023
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Facultative parthenogenesis: a transient state in transitions between sex and obligate asexuality in stick insects?

Facultative parthenogenesis and transitions from sexual to asexual reproduction

Recommended by ORCID_LOGO based on reviews by 3 anonymous reviewers

Despite a vast array of ways in which organisms can reproduce (Bell, 1982), most animals engage in sexual reproduction (Otto & Lenormand, 2002). A fascinating alternative to sex is parthenogenesis, where offspring are produced asexually from a gamete, typically the egg, without receiving genetic material from another gamete (Simon, Delmotte, Rispe, & Crease, 2003). One of the long-standing questions in the field is why parthenogenesis is not more widespread, given the costs associated with sex (Otto & Lenormand, 2002).  Natural populations of most species appear to be reproducing either sexually or parthenogenetically, even if a species can employ both reproductive modes (Larose et al 2023). Larose et al (2023) highlight the conundrum in this pattern, as organisms that are capable of employing parthenogenesis facultatively would be able to gain the benefits of both modes of reproduction. Why then, is facultative parthenogenesis not more common?

Larose et al (2023) propose that constraints on being efficient in both sexual and asexual reproduction could cause a trade-off between reproductive modes that favours an obligate strategy of either sex or no sex. This would provide an explanation for why facultative parthenogenesis is rare. Timema stick insects provide an excellent system to investigate reproductive strategies, as some species have parthenogenetic females, while other species are sexual, and they show repeated transitions from sexual reproduction to obligate parthenogenesis (Schwander & Crespi, 2009). The authors performed comprehensive and complementary studies in a recently discovered species T. douglasi, in which populations show both modes of reproduction, with some populations consisting only of females and others showing equal proportions of males and females. The sex ratio varied significantly, with the proportion of females ranging between 43-100% across 29 populations. These populations form a monophyletic clade with clustering into three genetic lineages and only a few cases of admixture. Females from all populations were capable of producing unfertilized eggs, but the hatching success varied hugely among populations and lineages (3-100%). Parthenogenetically produced offspring were homozygous, showing that parthenogenesis causes a complete loss of heterozygosity in a single generation. After producing eggs as virgins, females were mated to assess the capacity to also reproduce sexually, and fertilization increased the hatching success of eggs in two lineages. In one lineage, in which the hatching success of unfertilized eggs is similar to that of other sexually reproducing Timema species, fertilization reduced egg-hatching success, indicating a trade-off between reproductive modes with parthenogenetic reproduction performing best. Approximately 58% of the offspring produced after mating were fertilized, demonstrating the capacity of females to reproduce parthenogenetically also after mating has occurred, however with huge variation among individuals.

This wonderful and meticulously performed study produces strong and complementary evidence for facultative parthenogenesis in T. douglasi populations. The study shows large variation in how reproductive mode is employed, supporting the existence of a trade-off between sexual and parthenogenetic reproduction. This might be an example of an ongoing transition from sexual to asexual reproduction, which indicates that obligate parthenogenesis may derive via transient facultative parthenogenesis. 

REFERENCES

Bell, G. (1982) The Masterpiece of Nature: The Evolution and Genetics of Sexuality. University of California Press. 635 p.

Otto, S. P., & Lenormand, T. (2002). Resolving the paradox of sex and recombination. Nature Reviews Genetics, 3(4), 252-261. https://doi.org/10.1038/nrg761

Schwander, T., & Crespi, B. J. (2009). Multiple direct transitions from sexual reproduction to apomictic parthenogenesis in Timema stick insects. Evolution, 63(1), 84-103. 
https://doi.org/10.1111/j.1558-5646.2008.00524.x

Simon, J.-C., Delmotte, F., Rispe, C., & Crease, T. (2003). Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals. Biological Journal of the Linnean Society, 79(1), 151-163. https://doi.org/10.1046/j.1095-8312.2003.00175.x

Larose, C., Lavanchy,  G., Freitas, S., Parker, D.J., Schwander, T. (2023) Facultative parthenogenesis: a transient state in transitions between sex and obligate asexuality in stick insects? bioRxiv, 2022.03.25.485836, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.03.25.485836

Facultative parthenogenesis: a transient state in transitions between sex and obligate asexuality in stick insects?Chloé Larose, Guillaume Lavanchy, Susana Freitas, Darren J. Parker, Tanja Schwander<p>Transitions from obligate sex to obligate parthenogenesis have occurred repeatedly across the tree of life. Whether these transitions occur abruptly or via a transient phase of facultative parthenogenesis is rarely known. We discovered and char...Reproduction and SexTrine Bilde2022-05-20 10:41:13 View
30 Mar 2023
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Balancing selection at a wing pattern locus is associated with major shifts in genome-wide patterns of diversity and gene flow in a butterfly

Is genetic diversity enhanced by a supergene?

Recommended by based on reviews by Christelle Fraïsse and 2 anonymous reviewers

The butterfly species Heliconius numata has a remarkable wing pattern polymorphism, with multiple pattern morphs all controlled by a single genetic locus, which harbours multiple inversions. Each morph is a near-perfect mimic of a species in the fairly distantly related genus of butterflies, Melinaea.

The article by Rodríguez de Cara et al (2023) argues that the balanced polymorphism at this single wing patterning locus actually has a major effect on genetic diversity across the whole genome. First, polymorphic populations within H. numata are more dioverse than those without polymorphism. Second, H. numata is more genetically diverse than other related species and finally reconstruction of historical demography suggests that there has been a recent increase in effective population size, putatively associated with the acquisition of the supergene polymorphism. The supergene itself generates disassortative mating, such that morphs prefer to mate with others dissimilar to themselves - in this way it is similar to mechanisms for preventing inbreeding such as self-incompatibility loci in plants. This provides a potential mechanism whereby non-random mating patterns could increase effective population size. The authors also explore this mechanism using forward simulations, and show that mating patterns at a single locus can influence linked genetic diversity over a large scale.

Overall, this is an intriguing study, which suggests a far more widespread genetic impact of a single locus than might be expected. There are interesting parallels with mechanisms of inbreeding prevention in plants, such as the Pin/Thrum polymorphism in Primula, which also rely on mating patterns determined by a single locus but presumably also influence genetic diversity genome-wide by promoting outbreeding.

REFERENCES

Rodríguez de Cara MÁ, Jay P, Rougemont Q, Chouteau M, Whibley A, Huber B, Piron-Prunier F, Ramos RR, Freitas AVL, Salazar C, Silva-Brandão KL, Torres TT, Joron M (2023) Balancing selection at a wing pattern locus is associated with major shifts in genome-wide patterns of diversity and gene flow. bioRxiv, 2021.09.29.462348, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2021.09.29.462348

Balancing selection at a wing pattern locus is associated with major shifts in genome-wide patterns of diversity and gene flow in a butterflyMaría Ángeles Rodríguez de Cara, Paul Jay, Quentin Rougemont, Mathieu Chouteau, Annabel Whibley, Barbara Huber, Florence Piron-Prunier, Renato Rogner Ramos, André V. L. Freitas, Camilo Salazar, Karina Lucas Silva-Brandão, Tatiana Texeira Torres, M...<p style="text-align: justify;">Selection shapes genetic diversity around target mutations, yet little is known about how selection on specific loci affects the genetic trajectories of populations, including their genomewide patterns of diversity ...Evolutionary Ecology, Genome Evolution, Hybridization / Introgression, Population Genetics / GenomicsChris Jiggins2021-10-13 17:54:33 View
24 Mar 2023
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Domestication of different varieties in the cheese-making fungus Geotrichum candidum

Diverse outcomes in cheese fungi domestication

Recommended by ORCID_LOGO based on reviews by Delphine Sicard and 1 anonymous reviewer

Domestication is a complex process that imprints the demography and the genomes of domesticated populations, enforcing strong selective pressures on traits favourable to humans, e.g. for food production [1]. Domestication has been quite intensely studied in plants and animals, but less so in micro-organisms such as fungi, despite their assets (e.g. their small genomes and tractability in the lab). This elegant study by Bennetot and collaborators [2] on the cheese-making fungus Geotrichum candidum adds to the mounting body of studies in the genomics of fungi, proving they are excellent models in evolutionary biology for studying adaptation and drift in eukaryotes [3].

Bennetot et al. newly showed with whole genome sequences that all G. candidum strains isolated from cheese form a monophyletic clade subdivided into three genetically differentiated populations with several admixed strains, while the wild strains sampled from diverse geographic locations form a sister clade. This suggests the wild progenitor was not sampled in the present study and calls for future exciting work on the domestication history of the G. candidum fungus. The authors scanned the genomes for footprints of adaptation to the cheese environment and identified promising candidates, such as a gene involved in iron uptake (this element is limiting in cheese). Their functional genome analysis also provides evidence for higher contents of transposable elements in cheese-making strains, likely due to relaxed selection during the domestication process.

This paper is particularly impressive in that the authors complemented the population genomic approach with the phenotypic characterization of the strains and tested their ability to outcompete common fungal food spoilers. The authors convincingly showed that cheese-making strains display phenotypic differences relative to wild relatives for multiple traits such as slower growth, lower proteolysis activity and a greater amount of volatiles attractive to consumers, these phenotypes being beneficial for cheese making.

Finally, this work is particularly inspiring because it thoroughly discusses convergent evolution during domestication in different cheese-associated fungi. Indeed, studying populations experiencing similar environmental pressures is fundamental to understanding whether evolution is repeatable [4]. For instance, all three cheese populations of G. candidum exhibit a lower genetic diversity than wild populations. However, only one population displays a stronger domestication syndrome, resembling the Penicillium camemberti situation [5]. Furthermore, different cheese-making practices may have led to varying situations with clonal lineages in non-Roquefort P. roqueforti and P. camemberti [5, 6], while the cheese-making G. candidum populations still harbour some diversity. In a nutshell, Bennetot's study makes an important contribution to evolutionary biology and highlights the value of diversifying our model organisms toward under-represented clades.

REFERENCES

[1] Diamond J (2002) Evolution, consequences and future of plant and animal domestication. Nature 418: 700–707. https://doi.org/10.1038/nature01019

[2] Bennetot B, Vernadet J-P, Perkins V, Hautefeuille S, Rodríguez de la Vega RC, O’Donnell S, Snirc A, Grondin C, Lessard M-H, Peron A-C, Labrie S, Landaud S, Giraud T, Ropars J (2023) Domestication of different varieties in the cheese-making fungus Geotrichum candidum. bioRxiv, 2022.05.17.492043, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.05.17.492043 

[3] Gladieux P, Ropars J, Badouin H, Branca A, Aguileta G, de Vienne DM, Rodríguez de la Vega RC, Branco S, Giraud T (2014) Fungal evolutionary genomics provides insight into the mechanisms of adaptive divergence in eukaryotes. Mol. Ecol. 23: 753–773. https://doi.org/10.1111/mec.12631

[4] Bolnick DI, Barrett RD, Oke KB, Rennison DJ, Stuart YE (2018) (Non)Parallel evolution. Ann. Rev. Ecol. Evol. Syst. 49: 303–330. https://doi.org/10.1146/annurev-ecolsys-110617-062240 

[5] Ropars J, Didiot E, Rodríguez de la Vega RC, Bennetot B, Coton M, Poirier E, Coton E, Snirc A, Le Prieur S, Giraud T (2020) Domestication of the Emblematic White Cheese-Making Fungus Penicillium camemberti and Its Diversification into Two Varieties. Current Biol. 30: 4441–4453.e4. https://doi.org/10.1016/j.cub.2020.08.082

[6] Dumas, E, Feurtey, A, Rodríguez de la Vega, RC, Le Prieur S, Snirc A, Coton M, Thierry A, Coton E, Le Piver M, Roueyre D, Ropars J, Branca A, Giraud T (2020) Independent domestication events in the blue-cheese fungus Penicillium roqueforti. Mol Ecol. 29: 2639–2660. https://doi.org/10.1111/mec.15359

Domestication of different varieties in the cheese-making fungus *Geotrichum candidum*Bastien Bennetot, Jean-Philippe Vernadet, Vincent Perkins, Sophie Hautefeuille, Ricardo C. Rodríguez de la Vega, Samuel O’Donnell, Alodie Snirc, Cécile Grondin, Marie-Hélène Lessard, Anne-Claire Peron, Steve Labrie, Sophie Landaud, Tatiana Giraud,...<p>Domestication is an excellent model for studying adaptation processes, involving recent adaptation and diversification, convergence following adaptation to similar conditions, as well as degeneration of unused functions. <em>Geotrichum candidum...Adaptation, Genome Evolution, Population Genetics / GenomicsChristelle Fraïsse2022-08-12 20:50:42 View
16 Mar 2023
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Phylogeographic breaks and how to find them: Separating vicariance from isolation by distance in a lizard with restricted dispersal

The difficult task of partitioning the effects of vicariance and isolation by distance in poor dispersers

Recommended by ORCID_LOGO based on reviews by Kevin Sánchez and Aglaia (Cilia) Antoniou

Partitioning the effects of vicariance and low dispersal has been a long-standing problem in historical biogeography and phylogeography. While the term “vicariance” refers to divergence in allopatry, caused by some physical (geological, geographical) or climatic barriers (e.g. Rosen 1978), isolation by distance refers to the genetic differentiation of remote populations due to the physical distance separating them, when the latter surpasses the scale of dispersal (Wright 1938, 1940, 1943). 

Vicariance and dispersal have long been considered as separate forces leading to separate scenarii of speciation (e.g. reviewed in Hickerson and Meyer 2008). Nevertheless, these two processes are strongly linked, as, for example, vicariance theory relies on the assumption that ancestral lineages were once linked by dispersal prior to physical or climatic isolation (Rosen 1978). Low dispersal and vicariance are not mutually exclusive, and distinguishing these two processes in heterogeneous landscapes, especially for poor dispersers, remains therefore a severe challenge. For example, low dispersal (and/or small population size) can give rise to geographic patterns consistent with a phylogeographic break and be mistaken for geographic isolation (Irwin 2002, Kuo and Avise 2005).

The study of Rancilliac and colleagues (2023) is at the heart of this issue. It focuses on a nominal lizard species, the red-tailed spiny-footed lizard (Acanthodactylus erythrurus, Squamata: Lacertidae), which has a wide spatial distribution (from the Maghreb to the Iberian Peninsula), is found in a variety of different habitats, and has a wide range of morphological traits that do not always correlate with phylogeny. The main question is the following: have “the morphological and ecological diversification of this group been produced by vicariance and lineage diversification, or by local adaptation in the face of historical gene flow?” To tackle this question, the authors used sequence data from multiple mitochondrial and nuclear markers and a nested analysis workflow integrating phylogeography, multiple correspondence analyses and a relatively novel approach to IBD testing (Hausdorf & Henning, 2020). The latter is based on regression analysis and was shown to be less prone to error than the traditional (partial) Mantel test. 

While this set of methods allowed the partitioning of the effect of isolation by distance and vicariance in shaping contemporary genetic diversity in red-tailed spiny-footed lizards, some of the evolutionary history of this species complex remains blurred by ongoing gene flow and admixture, retention of ancestral polymorphism, or selection. The lack of congruence between mitochondrial and nuclear gene trees once again warns us that proposing evolutionary scenarii based on individual gene trees is a risky business. 

References

Hausdorf B, Hennig C (2020) Species delimitation and geography. Molecular Ecology Resources, 20, 950–960. https://doi.org/10.1111/1755-0998.13184

Hickerson MJ, Meyer CP (2008) Testing comparative phylogeographic models of marine vicariance and dispersal using a hierarchical Bayesian approach. BMC Evolutionary Biology, 8, 322. https://doi.org/10.1186/1471-2148-8-322

Irwin DE (2002) Phylogeographic breaks without geographic barriers to gene flow. Evolution, 56, 2383–2394. https://doi.org/10.1111/j.0014-3820.2002.tb00164.x

Kuo C-H, Avise JC (2005) Phylogeographic breaks in low-dispersal species: the emergence of concordance across gene trees. Genetica, 124, 179–186. https://doi.org/10.1007/s10709-005-2095-y

Rancilhac L, Miralles A, Geniez P, Mendez-Aranda D, Beddek M, Brito JC, Leblois R, Crochet P-A (2023) Phylogeographic breaks and how to find them: An empirical attempt at separating vicariance from isolation by distance in a lizard with restricted dispersal. bioRxiv, 2022.09.30.510256, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.09.30.510256

Rosen DE (1978) Vicariant Patterns and Historical Explanation in Biogeography. Systematic Biology, 27, 159–188. https://doi.org/10.2307/2412970

Wright, S (1938) Size of population and breeding structure in relation to evolution. Science 87:430-431.

Wright S (1940) Breeding Structure of Populations in Relation to Speciation. The American Naturalist, 74, 232–248. https://doi.org/10.1086/280891

Wright S (1943) Isolation by distance. Genetics, 28, 114–138. https://doi.org/10.1093/genetics/28.2.114

Phylogeographic breaks and how to find them: Separating vicariance from isolation by distance in a lizard with restricted dispersalLoïs Rancilhac, Aurélien Miralles, Philippe Geniez, Daniel Mendez-Arranda, Menad Beddek, José Carlos Brito, Raphaël Leblois, Pierre-André Crochet<p>Aim</p> <p>Discontinuity in the distribution of genetic diversity (often based on mtDNA) is usually interpreted as evidence for phylogeographic breaks, underlying vicariant units. However, a misleading signal of phylogeographic break can arise...Phylogeography & Biogeography, Population Genetics / Genomics, Speciation, Systematics / TaxonomyEric Pante Kevin Sánchez2022-10-05 13:11:28 View
06 Mar 2023
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Extrinsic mortality and senescence: a guide for the perplexed

Getting old gracefully, and risk of dying before getting there: a new guide to theory on extrinsic mortality and senescence

Recommended by and based on reviews by Nicole Walasek and 1 anonymous reviewer

Why is there such variation across species and populations in the rate at which individuals show wear and tear as they get older? Several compelling theoretical explanations have been developed on the conditions under which selection allows for or prevents senescence; a notable one being that proposed by George C Williams in 1957 based on the idea of antagonistic pleiotropy (Williams, 1957). One of the testable predictions of this theory is that, in populations where adults experience higher mortality, senescence is expected to be faster. This is one of the most influential predictions of the paper, being intuitive (when individuals are less likely to survive to later age classes, we expect weakened selection on traits that would avoid senescence in these classes), and fitting with ‘live fast, die young’ life history framing. As such, it has been widely incorporated into how we think about the evolution of senescence and has received considerable support in comparative studies across species and populations.  

However, it would be misleading to sit back at this point and think we have ‘solved’ the problem of understanding variation in senescence, and how this is linked with mortality. It turns out that the Williams 1957 paper is hotly contested by theoreticians: for the past 30 years – with increasing focus in the last 4 years – a growing body of models and opinion pieces have proposed flaws in the paper itself and in how it has been interpreted (Abrams, 1993; André and Rousset, 2020; Day and Abrams, 2020; Moorad et al., 2019). Central to several of these critiques is that explicit consideration of density dependence (not considered in Williams’ original paper) changes the conditions under which his predictions hold. A new preprint by de Vries, Gallipaud and Kokko brings further clarity to such critiques of the original paper (Vries et al., 2023). 

Beyond just continuing the tradition of critiquing Williams’ prediction, however, de Vries et al. provide a clear guide that is accessible to non-theoreticians about the issues with William’s prediction, and the way in which density dependence and how it operates can change when we expect senescence to occur. Rather than reiterate their points here, we suggest a close reading of the paper itself, along with an excellent overview of the paper in a recent blog by Daniel Nettle (Nettle, 2022). In brief, the paper starts by synthesizing earlier theoretical and empirical studies on the topic and presenting a very simple model to highlight how – in the absence of density dependence – Williams’ prediction does not hold because of the unregulated population growth, which is necessarily higher when there is low mortality. As a result, for a lineage with low mortality, any fitness advantage of placing offspring into the lineage later (i.e. selection for reduced senescence) is exactly cancelled out by the fact that earlier-produced offspring have higher fitness returns. 

They then present a more complex framework, which incorporates realistic mortality distributions, trade-offs between survival and reproduction, and use a series of 10 scenarios of density dependence (and whether this acts on survival or fecundity, and also whether it depends on a threshold or stochastic, or exerts continuing pressure on the trait) to explore selection on fitness-associated traits with age depending on extrinsic mortality. This then generates a range of results for when the Williams prediction holds, when there is no link between mortality and senescence, and when there is an ‘anti-Williams’ result – i.e., where senescence is slower when there is a high mortality. As has been shown in earlier studies, density dependence and how it operates matters, and Williams’ prediction holds most when density dependence affects juvenile age classes (in their model, when adults are less likely to produce them – i.e. there is density dependence on fecundity; or when there is less recruitment into the adult population due to, for example, competition among juveniles). 

So, perhaps we are now at a point where we can lay to rest the debate on the issues specifically with Williams’ original paper, and instead consider more broadly the key factors to measure when predicting patterns of senescence, and what is tangible for empiricists to quantify in their studies. Here, de Vries et al. provide some helpful insights both into the limitations of their approach and what modelling should be done moving forward, and into how we can link existing studies (for example comparing senescence among populations with varying predation pressure) to the theoretical predictions. At the heart of the latter is understanding the mechanism of density-dependent regulation – does it affect survival or fecundity, which age classes are most sensitive, and how do key traits depend on density? – and this is often difficult to measure in field studies.

And from all this we can learn that even very intuitive and extensively discussed concepts in biology do not always have as firm theoretical underpinnings as assumed, and – as should not be surprising – biology is complex and rather than one clear pattern being predicted, this can depend on a multitude of factors. 

REFERENCES

Abrams PA (1993) Does increased mortality favor the evolution of more rapid senescence? Evolution, 47, 877–887. https://doi.org/10.1111/j.1558-5646.1993.tb01241.x

André J-B, Rousset F (2020) Does extrinsic mortality accelerate the pace of life? A bare-bones approach. Evolution and Human Behavior, 41, 486–492. https://doi.org/10.1016/j.evolhumbehav.2020.03.002

Day T, Abrams PA (2020) Density Dependence, Senescence, and Williams’ Hypothesis. Trends in Ecology & Evolution, 35, 300–302. https://doi.org/10.1016/j.tree.2019.11.005

Moorad J, Promislow D, Silvertown J (2019) Evolutionary Ecology of Senescence and a Reassessment of Williams’ ‘Extrinsic Mortality’ Hypothesis. Trends in Ecology & Evolution, 34, 519–530. https://doi.org/10.1016/j.tree.2019.02.006

Nettle AD (2022) Live fast and die young (maybe). https://www.danielnettle.org.uk/2022/02/18/live-fast-and-die-young-maybe/ (accessed 2.27.23).

de Vries C, Galipaud M, Kokko H (2023) Extrinsic mortality and senescence: a guide for the perplexed. bioRxiv, 2022.01.27.478060, ver. 5 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.01.27.478060

Williams GC (1957) Pleiotropy, natural selection, and the evolution of senescence. Evolution, 11, 398–411. https://doi.org/10.1111/j.1558-5646.1957.tb02911.x

Extrinsic mortality and senescence: a guide for the perplexedCharlotte de Vries, Matthias Galipaud, Hanna Kokko<p style="text-align: justify;">Do environments or species traits that lower the mortality of individuals create selection for delaying senescence? Reading the literature creates an impression that mathematically oriented biologists cannot agree o...Evolutionary Dynamics, Evolutionary Ecology, Evolutionary Theory, Life HistorySinead English2022-08-26 14:30:16 View
28 Feb 2023
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Primate sympatry shapes the evolution of their brain architecture

Macroevolutionary drivers of brain evolution in primates

Recommended by based on reviews by Paula Gonzalez, Orlin Todorov and 3 anonymous reviewers

Studying the evolution of animal cognition is challenging because many environmental and species-related factors can be intertwined, which is further complicated when looking at deep-time evolution. Previous knowledge has emphasized the role of intraspecific interactions in affecting the socio-ecological environment shaping cognition. However, much less is known about such an effect at the interspecific level. Yet, the coexistence of different species in the same geographic area at a given time (sympatry) can impact the evolutionary history of species through character displacement due to biotic interactions. Trait evolution has been observed and tested with morphological external traits but more rarely with brain evolution. Compared to most species’ traits, brain evolution is even more delicate to assess since specific brain regions can be involved in different functions, may they be individual-based and social-based information processing. 

In a very original and thoroughly executed study, Robira & Perez-Lamarque (2023) addressed the question: How does the co-occurrence of congeneric species shape brain evolution and influence species diversification? By considering brain size as a proxy for cognition, they evaluated whether species sympatry impacted the evolution of cognition in frugivorous primates. Fruit resources are hard to find, not continuous through time, heterogeneously distributed across space, but can be predictable. Hence, cognition considerably shapes the foraging strategy and competition for food access can be fierce. Over long timescales, it remains unclear whether brain size and the pace of species diversification are linked in the context of sympatry, and if so how. Recent studies have found that larger brain sizes can be associated with higher diversification rates in birds (Sayol et al. 2019). Similarly, Robira & Perez-Lamarque (2023) thus wondered if the evolution of brain size in primates impacted their dynamic of species diversification, which has been suggested (Melchionna et al. 2020) but not tested.

Prior to anything, Robira & Perez-Lamarque (2023) had to retrace the evolutionary history of sympatry between frugivorous primate lineages through time using the primate tree of life, species’ extant distribution, and process-based models to estimate ancestral range evolution. To infer the effect of species sympatry on the evolution of cognition in frugivorous primates, the authors evaluated the support for phylogenetic models of brain size evolution accounting or not for species sympatry and investigated the directionality of the selection induced by sympatry on brain size evolution. Finally, to better understand the impact of cognition and interactions between primates on their evolutionary success, they tested for correlations between brain size or species’ sympatry and species diversification.

Robira & Perez-Lamarque (2023) found that the evolution of the whole brain or brain regions used in immediate information processing was best fitted with models not considering sympatry. By contrast, models considering species sympatry best predicted the evolution of brain regions related to long-term memory of interactions with the socio-ecological environment, with a decrease in their size along with stronger sympatry. Specifically, they found that sympatry was associated with a decrease in the relative size of the hippocampus and striatum, but had no significant effect on the neocortex, cerebellum, or overall brain size.

The hippocampus is a brain region that plays a crucial role in processing and memorizing spatiotemporal information, which is relevant for frugivorous primates in their foraging behavior. The study suggests that competition between sympatric species for limited food resources may lead to a more complex and unpredictable food distribution, which may in turn render cognitive foraging not advantageous and result in a selection for smaller brain regions involved in foraging. Niche partitioning and dietary specialization in sympatry may also impact cognitive abilities, with more specialized diets requiring lower cognitive abilities and smaller brain region sizes.

On the other hand, the absence of an effect of sympatry on brain regions involved in immediate sensory information processing, such as the cerebellum and neocortex, suggests that foragers do not exploit cues left out by sympatric heterospecific species, or they may discard environmental cues in favor of social cues.

This is a remarkable study that highlights the importance of considering the impact of ecological factors, such as sympatry, on the evolution of specific brain regions involved in cognitive processes, and the potential trade-offs in brain region size due to niche partitioning and dietary specialization in sympatry. Further research is needed to explore the mechanisms behind these effects and to test for the possible role of social cues in the evolution of brain regions. This study provides insights into the selective pressures that shape brain evolution in primates.

References

Melchionna M, Mondanaro A, Serio C, Castiglione S, Di Febbraro M, Rook L, Diniz-Filho JAF, Manzi G, Profico A, Sansalone G, Raia P (2020) Macroevolutionary trends of brain mass in Primates. Biological Journal of the Linnean Society, 129, 14–25. https://doi.org/10.1093/biolinnean/blz161

Robira B, Perez-Lamarque B (2023) Primate sympatry shapes the evolution of their brain architecture. bioRxiv, 2022.05.09.490912, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.05.09.490912

Sayol F, Lapiedra O, Ducatez S, Sol D (2019) Larger brains spur species diversification in birds. Evolution, 73, 2085–2093. https://doi.org/10.1111/evo.13811

Primate sympatry shapes the evolution of their brain architectureBenjamin Robira, Benoit Perez-Lamarque<p style="text-align: justify;">The main hypotheses on the evolution of animal cognition emphasise the role of conspecifics in affecting the socio-ecological environment shaping cognition. Yet, space is often simultaneously occupied by multiple sp...Behavior & Social Evolution, Bioinformatics & Computational Biology, Evolutionary Ecology, Macroevolution, Phylogenetics / Phylogenomics, Phylogeography & BiogeographyFabien Condamine2022-05-10 13:43:02 View
22 Feb 2023
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Increased birth rank of homosexual males: disentangling the older brother effect and sexual antagonism hypothesis

Evolutionary or proximal explanations for human male homosexual mate preference?

Recommended by ORCID_LOGO based on reviews by Ray Blanchard and 1 anonymous reviewer

Natural populations do not consist of only perfectly adapted individuals. If they did, of course, there would be no fodder for evolution by natural selection. And natural selection is operating all the time, winnowing out less well adapted phenotypes through differential reproduction and survival. Demonstrations of natural selection modifying characters-state distributions to bring phenotypes closer to their optima abound in the evolution literature, with examples of short- and long-term changes in phenotype and allele frequencies.  

However, evolutionary biologists know that populations cannot reach their adaptive peaks. Natural selection is tracking a moving target, always with some generations of lag time. The adaptive landscape is multidimensional, so the optimal combination of multiple character states may be impossible because of constraints and trade-offs. Natural selection does not operate alone or in isolation – new mutations and migrants that were selected under other conditions will inject locally non-adaptive genetic variation and genetic drift can change allele frequencies in random directions. We understand these processes that generate and maintain less advantageous variants on a continuous gradient from an optimal phenotype in a fitness landscape. More puzzling are heritable polymorphisms with distinct morphologies, physiologies or behaviours maintained in populations despite their measurably lower reproductive success. But a complete model of evolution must also be able to accommodate these Darwinian paradoxes.

Raymond et al. (2023) investigate one such Darwinian paradox: In humans, male homosexual mate preference is heritable and is associated with a large reduction in offspring production but nonetheless occurs at relatively high frequencies in most human populations. Furthermore, multiple studies have found that homosexual men come from families that are, on average, larger than those of heterosexual men and that homosexual men have, on average, higher birth rank than do heterosexual men, i.e., having more older siblings and, particularly, more older brothers. Two types of mechanisms consistent with these observations have been proposed: 1) An evolutionary mechanism of sex-antagonistic pleiotropy, whereby highly fecund mothers are more likely to produce homosexual sons, and 2) A mechanistic explanation whereby successive male pregnancies alter the uterine environment by increasing the probability of an immune reaction by the mother to her male fetus, altering development of sexually dimorphic brain structures relevant to sexual orientation.

In this article, the authors explore these two mechanisms of sex-antagonistic effects (AE) and fraternal birth order effects (FBOE) and test how well they account for patterns of male homosexuality in population and family data. Clearly, these two effects are somewhat confounded because high birth ranks can only occur in large families. If, indeed, the probability of male homosexuality increases with increasing numbers of (maternal) older brothers, homosexual males will be more common in larger families. Similarly, if high female fecundity leads to a higher probability of male homosexuality via sex-antagonistic effects, homosexual males will, on average, have more older brothers. To disentangle the actions of these two effects the authors modelled the relationship between birth rank and population fecundity and investigated whether AE or FBOE modified this relationship for homosexual men.  Simulation results were compared with aggregated population data from 13 countries.  Family data on individuals’ sexual preference, birth rank and number of male and female siblings from France, Greece and Indonesia were analysed with generalised linear models and Bayesian approaches to test for a signal of AE or FBOE. 

These analyses revealed a significant older-brother effect (FBOE) explaining patterns of occurrence of homosexuality in population and family data but no significant independent sex-antagonistic effect (AE). Thus larger family sizes of homosexual men appear due to the older-brother effect, with individuals of high birth rank coming necessarily from large sibships. The simulation approach also revealed that modelling a fraternal birth order effect (FBOE), such that individuals with more older brothers are more likely to be homosexual, generates an artefactual older sister effect simply because homosexual men are overrepresented at higher birth ranks. Older-sister effects reported in the literature may, therefore, be statistical artefacts of an underlying older-brother effect.

This paper is interesting for a number of reasons. It does an excellent job of explaining, identifying and dealing with estimation biases and testing for artefactual relationships generated by collinearity. It applies state-of-the art analytical/statistical tools. It breaks down two colinear effects and shows that only one really explains phenotypic variation. This is a great example of how to disentangle correlated variables that may or may not both contribute to trait variation. But most intriguingly, we are left without evidence for an evolutionary mechanism that compensates the large fitness cost associated with male homosexuality in humans. How can we explain high heritability maintained in the face of strong directional selection that should erode heritable genetic variation? The usual suspects include cryptic compensatory mechanisms yet to be discovered or flawed estimates of selection or heritability. For example, data on heritability of male homosexual mate preference in humans come from twin studies and twins share birth rank as well as alleles. Thus it is possible that heritability is over-estimated, including the environmental component associated with birth rank. 

If, as the authors demonstrate here, birth rank is the strongest predictor of male homosexual mate preference, selection may be acting on a non-heritable plastic component of phenotypic variation. This could explain why heritable variation is not exhausted by selection, rendering the paradox less paradoxical, but fails to provide an adaptive explanation for the maintenance of male homosexual mate preference. 

References

Raymond M., Turek D., Durand V., Nila S., Suryobroto B., Vadez J., Barthes J., Apostolou M. and Crochet P.-A. (2023) Increased birth rank of homosexual males: disentangling the older brother effect and sexual antagonism hypothesis. bioRxiv, 2022.02.22.481477, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.02.22.481477

Increased birth rank of homosexual males: disentangling the older brother effect and sexual antagonism hypothesisMichel Raymond, Daniel Turek, Valerie Durand, Sarah Nila, Bambang Suryobroto, Julien Vadez, Julien Barthes, Menelaos Apostolou, Pierre-André Crochet<p style="text-align: justify;">Male homosexual orientation remains a Darwinian paradox, as there is no consensus on its evolutionary (ultimate) determinants. One intriguing feature of homosexual men is their higher male birth rank compared to het...Life History, Other, Phenotypic Plasticity, Reproduction and SexJacqui A. Shykoff2022-03-03 11:28:44 View