Molecular phylogeny and evolution in vertebrates

Juan Ignacio Montoya-Burgos

Lecturer

  • T: +41 22 379 67 86
  • office 4067b (Sciences III)

We are interested in understanding how the biodiversity that is surrounding us has originated and is maintained. We approach this wide subject by conducting several well-defined research lines that examine the role played by extrinsic factors such as allopatric divergence, past climatic or environmental changes or the introduction of invasive species by humans. We also analyze how intrinsic factors may drive new diversity like adaptation to new environments, the emergence of selectively advantageous traits, or the ability to have an accelerated substitution rate. In parallel, we develop new bioinformatics or laboratory methods to facilitate our investigations. We use a wide panel of techniques, approaches and methods that range from field experiments to genome sequencing, assembly and annotation.

Our Softwares

LS3 PSGfinder LSX

Selected references

Rivera-Rivera and Montoya-Burgos. 2017. LSX: Automated reduction of gene-specific lineage evolutionary rate heterogeneity for multi-gene phylogeny inference. bioRxiv https://www.biorxiv.org/content/early/2017/11/16/220053.

Rivera-Rivera CJ, Montoya-Burgos JI 2017. Trunk dental tissue evolved independently from underlying dermal bony plates but is associated with surface bones in living odontode-bearing catfish. Proc. Biol. Sci. 2017 Oct; 284(1865).

Rivera-Rivera, C. J., Montoya-Burgos, J. I. 2016. LS³: A method for improving phylogenomic inferences when evolutionary rates are heterogeneous among Taxa. Molecular Biology and Evolution 33(6):1625-34.

Quilodran, C., Montoya-Burgos*, J. I., Currat, M. 2015. Modelling interspecific hybridization with genome exclusion to identify conservation actions: the case of native and invasive Pelophylax waterfrogs. Evolutionary Applications 8(2):199-210.
* Corresponding author

Quilodran, C., Currat, M., Montoya-Burgos, J. I. 2014. A General Model of Distant Hybridization Reveals the Conditions for Extinction in Atlantic Salmon and Brown Trout. PLoSONE 9(7): e101736.

Cardoso, Y. P., Almiron, A., Casciotta, J., Aichino, D., Lizarralde, M. S., Montoya- Burgos, J. I. 2012.Origin and species diversity in the catfish genus Hypostomus (Siluriformes: Loricariidae) inhabiting Argentinean río Paraná basin, with the description of a new species. Zootaxa 3453:69-83.

Surget-Groba, Y., Montoya-Burgos, J. I. 2010. Optimization of de novo transcriptome assembly from next-generation sequencing data. Genome Research 20:1432-1440.

Cardoso, Y. P., and Montoya-Burgos, J. I. 2009. Unexpected diversity in the catfish Pseudancistrus brevispinis reveals dispersal routes in a Neotropical center of endemism: the Guyanas Region. Molecular Ecology 18:947-964.

Montoya-Burgos, J. I., Foulon, A., and Bahechar, I. A. 2009. Transcriptome screen for fast evolving genes by Inter-Specific Selective Hybridization (ISSH). BMC Genomics 11:126.

Current projects

Interspecific hybridization: its impact on ecology, evolution and conservation

Post-doc : Claudio Quilodrán

Natural hybridization has played an important role in the evolution of many plant and animal taxa. However, when hybridization is caused by anthropogenic factors, it may lead to serious consequences for parental species persistance. This is particularly true in rare or threatened species, because if the population size is too small, their genotype may be gradually replaced by that of hybrids. This research project aims at modeling interspecific hybridization in order to evaluate its impact on the demography, ecology, and evolution of the parental species. We highlight the potential effects of exotic invasive species and habitat modifications, in particular due to global climate change. Our models offer a tool to estimate under which conditions the increasing rate of hybridization can represent a threat to species persistance and to provide guidance when choosing alternative conservation strategies.

Funding :

  • Center for Advanced Modeling Science (CADMOS), Switzerland
  • Institute of Genetics and Genomics of Geneva (iGE3)

 

Paleoclimactic changes and Neotropical fish diversification

Post-doc : Yamila C. Cardoso

In South America, the Plio-Pleistocene epoch was characterized by cycles of dry to humid climatic changes of large amplitude. Our working hypothesis states that during the driest periods, the water flow of rivers may have been reduced up to the point of disconnecting some tributaries from the rest of the basin, whereas a reconnection was achieved during the next humid period. This fragmentation-reconnection dynamic may have persisted throughout the climatic fluctuations of the Plio-Pleistocene. In Argentina, the arid Northwestern region of the La Plata basin displays a number of disconnected tributaries that mimic the postulated situation of many Neotropical river basins during the dry epochs of the Plio-Pleistocene. To test our hypothesis, we are inferring and analyzing the evolutionary history of selected freshwater fish taxa that we collected in several isolated tributaries as well as in the main course of the Paraguay and Paraná rivers, belonging to the La Plata basin.

Funding :

  • Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina
  • Swiss bilateral science & technology cooperation program, Argentina, SNSF - EPFL

 

Methodology in Molecular Phylogenetics

PhD student : Carlos J. Rivera-Rivera

The swift advance of gene sequencing technologies has produced a flood of data that we can use to infer evolutionary relationships among organisms. However, the staggering pace at which these data are produced surpasses the pace at which methods for their analysis are developed. This often leaves us using tools that are not fit for analyzing all of our data. In this project, we are interested in developing algorithms of data filtering that tailor these large-scale datasets to better fit the limitations of the methods we have available today. In this way, the information that is extracted from these data is clear, and the effect of noise and of misinterpreted signals is reduced.

Funding :

  • Swiss National Science Foundations (SNF)
  • Institute of Genetics and Genomics of Geneva (iGE3)

 

An exoskeleton covered with teeth

PhD student : Carlos J. Rivera-Rivera

Most vertebrates have teeth in their mouth to process their food. However, in a very curious groups of Neotropical catfishes, the Loricariidae, teeth can be found not only in the mouth, but also all over their bodies. These extra-oral teeth (odontodes) are arranged on their body surface, including their fin rays, and are an integral part of an intricate exoskeletal system that also includes dermal bony plates. We hypothesize that this protective and spiny exoskeleton is a key determinant of the tremendous species-richness of the groups with this trait. We use developmental and genetic approaches to find the genes and gene expression regulators that allowed the formation of these skeletal and dental structures in such an unlikely place as the trunk.

Funding :

  • Swiss National Science Foundations (SNF)
  • Institute of Genetics and Genomics of Geneva (iGE3)

 

Drivers of fish diversification in the Neotropics

PhD student : Luiz Jardim de Queiroz

Why do tropical regions of the world harbor the vast majority of Earth’s biodiversity? This is the basic question underlying our research project on ichthyological biodiversity in Tropical South America. This project is aimed at understanding how evolutionary and ecological processes have shaped the current fish diversity in the Neotropics. To gain some insights into this very challenging topic, three research lines are developed. First, factors of diversification at the intra-specific level are investigated by applying approaches from ecological and population landscape genetics to the case of the Amazonian sardine, Triportheus albus, as a model species. Second, we infer the diversification history of the endemic and species-rich catfish genus Hypostomus across South America. By combining calibrated phylogenies, morphological and ecological ancestral traits reconstructions and historical biogeography, we aim at unraveling the processes that shaped diversification at the species level. Third, we conduct a comparative transcriptomic study to examine the role played by adaptive evolution in traits that may explain species survival and diversification in the Neotropical region, such as resistance to hypoxia and to warm water temperatures.

This research project is performed in collaboration with colleagues from Brazilian and Argentinean institutions, and from the Museum of Natural History of Geneva.

Funding :

  • Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brazil
  • Brazilian-Swiss joint Research Programme (BSJRP) grant, SNSF - EPFL

 

How can population size and structure influence genome evolution?

Master student : Elisabeth Bizet

In this project we address the issue of how genome evolution is affected by micro-evolutionary factors such as population structure and effective population size. We use empirical observations and data taken from the literature to draw hypotheses. We then examine our hypotheses using population simulation approaches.

 

A fast method to identify genes under positive selection: DWin and PSGfinder

Current master student : Céline Adam

Genes evolving under positive Darwinian selection are expected to be involved in the evolution of adaptive traits. With the rapid increase of genomic data, it becomes possible to build the catalogue of positively selected genes (PSG) in a species, but current methods for identifying PSGs are too conservative and rather slow. This project is aimed at developing a fast and accurate method (DWin) to screen a collection of protein-coding genes belonging to a pair or a triplet of related species in search of PSGs. Our method is implemented in the software PSGfinder, which is being tested on well-characterized sets of genes that have experienced episodes of positive selection along the evolution of cetaceans. The PSGfinder software was the training work of a former master student, Joël Tuberosa, and it was partly tested in Weber et al. (2017).

The current reference for the PSGfinder software is: Tuberosa J., Juan I. Montoya-Burgos J. I. 2017. PSGfinder: fast identification of genes under divergent positive selection using the dynamic windows method. bioRxiv 193722; doi: https://doi.org/10.1101/193722.

 

Assembling the genome of a Loricariidae

Master student : David Dreifuss

With about 900 valid species, the Loricariidae is the most diversified freshwater fish family endemic to the Neotropics. Taking advantage of next-generation DNA sequencing technologies and our laboratory’s expertise in bioinformatics, we are now sequencing and assembling the genome of one representative, Ancistrus dolichopterus. This annotated new genome will serve to investigate the intrinsic determinants of the tremendous species diversity found in this family.

  • Effect of hybridization with genome exclusion on extinction risk. Conserv. Biol. 2018 Apr;():. 10.1111/cobi.13120.

    abstract

    Human-induced habitat changes may lead to the breakdown of reproductive barriers between distantly related species. This phenomenon may result in fertile first-generation hybrids (F ) that exclude the genome of one parental species during gametogenesis, thus disabling introgression. The species extinction risk associated with hybridization with genome exclusion is largely underappreciated because the phenomenon produces only F hybrid phenotype, leading to the misconception that hybrids are sterile and potentially of minor conservation concern. We used a simulation model that integrates the main genetic, demographic, and ecological processes to examine the dynamics of hybridization with genome exclusion. We showed that this mode of hybridization may lead to extremely rapid extinction when the process of genome exclusion is unbalanced between the interbreeding species and when the hybridization rate is not negligible. The coexistence of parental species was possible in some cases of asymmetrical genome exclusion, but show this equilibrium was highly vulnerable to environmental variation. Expanding the exclusive habitat of the species at risk allowed its persistence. Our results highlight the extent of possible extinction risk due to hybridization with genome exclusion and suggest habitat management as a promising conservation strategy. In anticipation of serious threats to biodiversity due to hybridization with genome exclusion, we recommend a detailed assessment of the reproductive status of hybrids in conservation programs. We suggest such assessments include the inspection of genetic content in hybrid gametes.

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  • The contribution of neutral evolution and adaptive processes in driving phenotypic divergence in a model mammalian species, the Andean fox Lycalopex culpaeus Journal of Biogeography. 2018;45:1114–1125

    abstract

    Understanding the mechanisms that drive phenotypic divergence along climatic gradients is a long‐standing goal of biogeography. To fulfil this objective, we tested if neutral and/or adaptive effects drive phenotypic diversification. We quantified the effects of neutral evolution and natural selection on morphological variability of a well‐suited mammalian species, the fox, Lycalopex culpaeus.

    see on external website

  • Cryptic Biological Invasions: a General Model of Hybridization. Sci Rep 2018 Feb;8(1):2414. 10.1038/s41598-018-20543-6. 10.1038/s41598-018-20543-6.

    abstract

    The dispersal of non-native genes due to hybridization is a form of cryptic invasion with growing concern in evolution and conservation. This includes the spread of transgenic genes and antibiotic resistance. To investigate how genes and phenotypes are transmitted, we developed a general model that, for the first time, considers concurrently: multiple loci, quantitative and qualitative gene expression, assortative mating, dominance/recessivity inheritance and density-dependent demographic effects. Selection acting on alleles or genotypes can also be incorporated. Our results reveal that the conclusions about how hybridization threatens a species can be biased if they are based on single-gene models, while considering two or more genes can correct this bias. We also show that demography can amplify or balance the genetic effects, evidencing the need of jointly incorporating both processes. By implementing our model in a real case, we show that mallard ducks introduced in New Zealand benefit from hybridization to replace native grey-ducks. Total displacement can take a few generations and occurs by interspecific competition and by competition between hybrids and natives, demonstrating how hybridization may facilitate biological invasions. We argue that our general model represents a powerful tool for the study of a wide range of biological and societal questions.

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  • Multifactorial genetic divergence processes drive the onset of speciation in an Amazonian fish. PLoS ONE 2017 ;12(12):e0189349. 10.1371/journal.pone.0189349. PONE-D-17-12071.

    abstract

    Understanding the processes that drive population genetic divergence in the Amazon is challenging because of the vast scale, the environmental richness and the outstanding biodiversity of the region. We addressed this issue by determining the genetic structure of the widespread Amazonian common sardine fish Triportheus albus (Characidae). We then examined the influence, on this species, of all previously proposed population-structuring factors, including isolation-by-distance, isolation-by-barrier (the Teotônio Falls) and isolation-by-environment using variables that describe floodplain and water characteristics. The population genetics analyses revealed an unusually strong structure with three geographical groups: Negro/Tapajós rivers, Lower Madeira/Central Amazon, and Upper Madeira. Distance-based redundancy analyses showed that the optimal model for explaining the extreme genetic structure contains all proposed structuring factors and accounts for up to 70% of the genetic structure. We further quantified the contribution of each factor via a variance-partitioning analysis. Our results demonstrate that multiple factors, often proposed as individual drivers of population divergence, have acted in conjunction to divide T. albus into three genetic lineages. Because the conjunction of multiple long-standing population-structuring processes may lead to population reproductive isolation, that is, the onset of speciation, we suggest that the multifactorial population-structuring processes highlighted in this study could account for the high speciation rate characterising the Amazon Basin.

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  • LSX: Automated reduction of gene-specific lineage evolutionary rate heterogeneity for multi-gene phylogeny inference bioRxiv: November 16, 2017. doi: https://doi.org/10.1101/220053

    abstract

    Motivation: LS3 is a recently published algorithm to reduce lineage evolutionary rate heterogeneity, a condition that can produce inference artifacts in molecular phylogenetics. The LS3 scripts are Linux-specific and the criterion to reduce lineage rate heterogeneity can be too stringent in datasets with both very long and very short branches. Results: LSX is a multi-platform user-friendly R script that performs the LS3 algorithm, and has added features in order to make better lineage rate calculations. In addition, we developed and implemented an alternative version of the algorithm, LS4, which reduces lineage rate heterogeneity not only by detecting branches that are too long but also branches that are too short, resulting in less stringent data filtering. Availability: The LSX script LSx_v.1.1.R and the user manual are available for download at: https://genev.unige.ch/research/laboratory/Juan-Montoya .

    see on external website

  • Trunk dental tissue evolved independently from underlying dermal bony plates but is associated with surface bones in living odontode-bearing catfish. Proc. Biol. Sci. 2017 Oct;284(1865):. rspb.2017.1831. 10.1098/rspb.2017.1831.

    abstract

    Although oral dental tissue is a vertebrate attribute, trunk dental tissue evolved in several extinct vertebrate lineages but is rare among living species. The question of which processes trigger dental-tissue formation in the trunk remains open, and would shed light on odontogenesis evolution. Extra-oral dental structures (odontodes) in the trunk are associated with underlying dermal bony plates, leading us to ask whether the formation of trunk bony plates is necessary for trunk odontodes to emerge. To address this question, we focus on Loricarioidei: an extant, highly diverse group of catfish whose species all have odontodes. We examined the location and cover of odontodes and trunk dermal bony plates for all six loricarioid families and 17 non-loricarioid catfish families for comparison. We inferred the phylogeny of Loricarioidei using a new 10-gene dataset, eight time-calibration points, and noise-reduction techniques. Based on this phylogeny, we reconstructed the ancestral states of odontode and bony plate cover, and find that trunk odontodes emerged before dermal bony plates in Loricarioidei. Yet we discovered that when bony plates are absent, other surface bones are always associated with odontodes, suggesting a link between osteogenic and odontogenic developmental pathways, and indicating a remarkable trunk odontogenic potential in Loricarioidei.

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  • Risks associated with introduction of poeciliids for control of mosquito larvae: first record of the non-native Gambusia holbrooki in Argentina. J. Fish Biol. 2017 Jul;():. 10.1111/jfb.13370.

    abstract

    This study confirms the presence of two species of the non-native mosquitofish Gambusia in Argentina. The risks that they represent to native biota, their potential dispersal in the region, and their effectiveness in mosquito larvae control are discussed.

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  • Morphological and ecological divergence in South American canids J. Biogeogr., 44: 821–833. doi:10.1111/jbi.12984

    abstract

    Closely related species are expected to be similar in their ecological attributes. However, clades colonizing new environments and diversifying due to ecological processes often show morphological and ecological divergence. Canids arrived in South America after the formation of the Isthmus of Panama and diversified to occupy a variety of habitats. We test whether the diversification of this group was followed by divergence in species niches. If ecological processes are associated with species divergences, we expect to see species occupying distinct climatic niches, showing divergent phenotypes, and showing a close association between their phenotypes and ecological attributes.

    see on external website

  • Positive selection on sperm ion channels in a brooding brittle star: consequence of life-history traits evolution. Mol. Ecol. 2017 Jan;():. 10.1111/mec.14024.

    abstract

    Closely related species are key models to investigate mechanisms leading to reproductive isolation and early stages of diversification, also at the genomic level. The brittle star cryptic species complex Ophioderma longicauda encompasses the sympatric broadcast spawning species C3 and the internal brooding species C5. Here we used de novo transcriptome sequencing and assembly in two closely related species displaying contrasting reproductive modes to compare their genetic diversity and to investigate the role of natural selection in reproductive isolation. We reconstructed 20,146 and 22,123 genes for C3 and C5, respectively, and characterized a set of 12,229 orthologs. Genetic diversity was 1.5-2 times higher in C3 compared to C5, confirming that species with low parental investment display higher levels of genetic diversity. Forty-eight genes were the targets of positive diversifying selection during the evolution of the two species. Notably, two genes (NHE and TetraKCNG) are sperm-specific ion channels involved in sperm motility. Ancestral sequence reconstructions show that natural selection targeted the two genes in the brooding species. This may result from an adaptation to the novel environmental conditions surrounding sperm in the brooding species, either directly affecting sperm, or via an increase in male/female conflict. This phenomenon could have promoted prezygotic reproductive isolation between C3 and C5. Finally, the sperm receptors to egg chemoattractants differed between C3 and C5 in the ligand-binding region. We propose that mechanisms of species-specific gamete recognition in brittle stars occur during sperm chemotaxis (sperm attraction towards the eggs), contrary to other marine invertebrates where prezygotic barriers to interspecific hybridization typically occur before sperm-egg fusion. This article is protected by copyright. All rights reserved.

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  • LS³: A Method for Improving Phylogenomic Inferences When Evolutionary Rates Are Heterogeneous among Taxa. Mol. Biol. Evol. 2016 Jun;33(6):1625-34. msw043. 10.1093/molbev/msw043. PMC4868118.

    abstract

    Phylogenetic inference artifacts can occur when sequence evolution deviates from assumptions made by the models used to analyze them. The combination of strong model assumption violations and highly heterogeneous lineage evolutionary rates can become problematic in phylogenetic inference, and lead to the well-described long-branch attraction (LBA) artifact. Here, we define an objective criterion for assessing lineage evolutionary rate heterogeneity among predefined lineages: the result of a likelihood ratio test between a model in which the lineages evolve at the same rate (homogeneous model) and a model in which different lineage rates are allowed (heterogeneous model). We implement this criterion in the algorithm Locus Specific Sequence Subsampling (LS³), aimed at reducing the effects of LBA in multi-gene datasets. For each gene, LS³ sequentially removes the fastest-evolving taxon of the ingroup and tests for lineage rate homogeneity until all lineages have uniform evolutionary rates. The sequences excluded from the homogeneously evolving taxon subset are flagged as potentially problematic. The software implementation provides the user with the possibility to remove the flagged sequences for generating a new concatenated alignment. We tested LS³ with simulations and two real datasets containing LBA artifacts: a nucleotide dataset regarding the position of Glires within mammals and an amino-acid dataset concerning the position of nematodes within bilaterians. The initially incorrect phylogenies were corrected in all cases upon removing data flagged by LS³.

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  • Molecular phylogeny of the highly diversified catfish subfamily Loricariinae (Siluriformes, Loricariidae) reveals incongruences with morphological classification. Mol. Phylogenet. Evol. 2016 Jan;94(Pt B):492-517. S1055-7903(15)00321-8. 10.1016/j.ympev.2015.10.018.

    abstract

    The Loricariinae belong to the Neotropical mailed catfish family Loricariidae, the most species-rich catfish family. Among loricariids, members of the Loricariinae are united by a long and flattened caudal peduncle and the absence of an adipose fin. Despite numerous studies of the Loricariidae, there is no comprehensive phylogeny of this morphologically highly diversified subfamily. To fill this gap, we present a molecular phylogeny of this group, including 350 representatives, based on the analysis of mitochondrial and nuclear genes (8426 positions). The resulting phylogeny indicates that Loricariinae are distributed into two sister tribes: Harttiini and Loricariini. The Harttiini tribe, as classically defined, constitutes a paraphyletic assemblage and is here restricted to the three genera Harttia, Cteniloricaria, and Harttiella. Two subtribes are distinguished within Loricariini: Farlowellina and Loricariina. Within Farlowellina, the nominal genus formed a paraphyletic group, as did Sturisoma and Sturisomatichthys. Within Loricariina, Loricaria, Crossoloricaria, and Apistoloricaria are also paraphyletic. To solve these issues, and given the lack of clear morphological diagnostic features, we propose here to synonymize several genera (Quiritixys with Harttia; East Andean members of Crossoloricaria, and Apistoloricaria with Rhadinoloricaria; Ixinandria, Hemiloricaria, Fonchiiichthys, and Leliella with Rineloricaria), to restrict others (Crossoloricaria, and Sturisomatichthys to the West Andean members, and Sturisoma to the East Andean species), and to revalidate the genus Proloricaria.

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  • Modelling interspecific hybridization with genome exclusion to identify conservation actions: the case of native and invasive Pelophylax waterfrogs. Evol Appl 2015 Feb;8(2):199-210. 10.1111/eva.12245. PMC4319866.

    abstract

    Interspecific hybridization occurs in nature but can also be caused by human actions. It often leads to infertile or fertile hybrids that exclude one parental genome during gametogenesis, escaping genetic recombination and introgression. The threat that genome-exclusion hybridization might represent on parental species is poorly understood, especially when invasive species are involved. Here, we show how to assess the effects of genome-exclusion hybridization and how to elaborate conservation actions by simulating scenarios using a model of nonintrogressive hybridization. We examine the case of the frog Pelophylax ridibundus, introduced in Western Europe, which can hybridize with the native Pelophylax lessonae and the pre-existing hybrid Pelophylax esculentus, maintained by hybridogenesis. If translocated from Southern Europe, P. ridibundus produces new sterile hybrids and we show that it mainly threatens P. esculentus. Translocation from Central Europe leads to new fertile hybrids, threatening all native waterfrogs. Local extinction is demographically mediated via wasted reproductive potential or via demographic flow through generations towards P. ridibundus. We reveal that enlarging the habitat size of the native P. lessonae relative to that of the invader is a promising conservation strategy, avoiding the difficulties of fighting the invader. We finally stress that nonintrogressive hybridization is to be considered in conservation programmes.

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  • A general model of distant hybridization reveals the conditions for extinction in Atlantic salmon and brown trout. PLoS ONE 2014 ;9(7):e101736. 10.1371/journal.pone.0101736. PONE-D-14-07667. PMC4086968.

    abstract

    Interspecific hybridization is common in nature but can be increased in frequency or even originated by human actions, such as species introduction or habitat modification, which may threaten species persistence. When hybridization occurs between distantly related species, referred to as "distant hybridization," the resulting hybrids are generally infertile or fertile but do not undergo chromosomal recombination during gametogenesis. Here, we present a model describing this frequent but poorly studied interspecific hybridization to assess its consequences on parental species and to anticipate the conditions under which they can reach extinction. Our general model fully incorporates three important processes: density-dependent competition, dominance/recessivity inheritance of traits and assortative mating. We demonstrate its use and flexibility by assessing population extinction risk between Atlantic salmon and brown trout in Norway, whose interbreeding has recently increased due to farmed fish releases into the wild. We identified the set of conditions under which hybridization may threaten salmonid species. Thanks to the flexibility of our model, we evaluated the effect of an additional risk factor, a parasitic disease, and showed that the cumulative effects dramatically increase the extinction risk. The consequences of distant hybridization are not genetically, but demographically mediated. Our general model is useful to better comprehend the evolution of such hybrid systems and we demonstrated its importance in the field of conservation biology to set up management recommendations when this increasingly frequent type of hybridization is in action.

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  • Patterns of positive selection and neutral evolution in the protein-coding genes of Tetraodon and Takifugu. PLoS ONE 2011 ;6(9):e24800. 10.1371/journal.pone.0024800. PONE-D-11-06907. PMC3172292.

    abstract

    Recent genome-wide analyses have revealed patterns of positive selection acting on protein-coding genes in humans and mammals. To assess whether the conclusions drawn from these analyses are valid for other vertebrates and to identify mammalian specificities, I have investigated the selective pressure acting on protein-coding genes of the puffer fishes Tetraodon and Takifugu. My results indicate that the strength of purifying selection in puffer fishes is similar to previous reports for murids but stronger in hominids, which have a smaller population size. Gene ontology analyses show that more than half of the biological processes targeted by positive selection in mammals are also targeted in puffer fishes, highlighting general patterns for vertebrates. Biological processes enriched with positively selected genes that are shared between mammals and fishes include immune and defense responses, signal transduction, regulation of transcription and several of their descendent terms. Mammalian-specific processes displaying an excess of positively selected genes are related to sensory perception and neurological processes. The comparative analyses also revealed that, for both mammals and fishes, genes encoding extracellular proteins are preferentially targeted by positive selection, indicating that adaptive evolution occurs more often in the extra-cellular environment rather than inside the cell. Moreover, I present here the first genome-wide characterization of neutrally-evolving regions of protein-coding genes. This analysis revealed an unexpectedly high proportion of genes containing both positively selected motifs and neutrally-evolving regions, uncovering a strong link between neutral evolution and positive selection. I speculate that neutrally-evolving regions are a major source of novelties screened by natural selection.

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  • Optimization of de novo transcriptome assembly from next-generation sequencing data. Genome Res. 2010 Oct;20(10):1432-40. gr.103846.109. 10.1101/gr.103846.109. PMC2945192.

    abstract

    Transcriptome analysis has important applications in many biological fields. However, assembling a transcriptome without a known reference remains a challenging task requiring algorithmic improvements. We present two methods for substantially improving transcriptome de novo assembly. The first method relies on the observation that the use of a single k-mer length by current de novo assemblers is suboptimal to assemble transcriptomes where the sequence coverage of transcripts is highly heterogeneous. We present the Multiple-k method in which various k-mer lengths are used for de novo transcriptome assembly. We demonstrate its good performance by assembling de novo a published next-generation transcriptome sequence data set of Aedes aegypti, using the existing genome to check the accuracy of our method. The second method relies on the use of a reference proteome to improve the de novo assembly. We developed the Scaffolding using Translation Mapping (STM) method that uses mapping against the closest available reference proteome for scaffolding contigs that map onto the same protein. In a controlled experiment using simulated data, we show that the STM method considerably improves the assembly, with few errors. We applied these two methods to assemble the transcriptome of the non-model catfish Loricaria gr. cataphracta. Using the Multiple-k and STM methods, the assembly increases in contiguity and in gene identification, showing that our methods clearly improve quality and can be widely used. The new methods were used to assemble successfully the transcripts of the core set of genes regulating tooth development in vertebrates, while classic de novo assembly failed.

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  • Changes in Hox genes' structure and function during the evolution of the squamate body plan. Nature 2010 Mar;464(7285):99-103. nature08789. 10.1038/nature08789.

    abstract

    Hox genes are central to the specification of structures along the anterior-posterior body axis, and modifications in their expression have paralleled the emergence of diversity in vertebrate body plans. Here we describe the genomic organization of Hox clusters in different reptiles and show that squamates have accumulated unusually large numbers of transposable elements at these loci, reflecting extensive genomic rearrangements of coding and non-coding regulatory regions. Comparative expression analyses between two species showing different axial skeletons, the corn snake and the whiptail lizard, revealed major alterations in Hox13 and Hox10 expression features during snake somitogenesis, in line with the expansion of both caudal and thoracic regions. Variations in both protein sequences and regulatory modalities of posterior Hox genes suggest how this genetic system has dealt with its intrinsic collinear constraint to accompany the substantial morphological radiation observed in this group.

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  • Transcriptome screen for fast evolving genes by Inter-Specific Selective Hybridization (ISSH). BMC Genomics 2010 ;11():126. 1471-2164-11-126. 10.1186/1471-2164-11-126. PMC2838844.

    abstract

    Fast evolving genes are targets of an increasing panel of biological studies, from cancer research to population genetics and species specific adaptations. Yet, their identification and isolation are still laborious, particularly for non-model organisms. We developed a method, named the Inter-Specific Selective Hybridization (ISSH) method, for generating cDNA libraries enriched in fast evolving genes. It utilizes transcripts of homologous tissues of distinct yet related species. Experimental hybridization conditions are monitored in order to discard transcripts that do not find their homologous counterparts in the two species sets as well as transcripts that display a strong complementarity between the two species. Only heteroduplexes that disanneal at low stringency are used for constructing the resulting cDNA library.

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  • Atypical relaxation of structural constraints in Hox gene clusters of the green anole lizard. Genome Res. 2009 Apr;19(4):602-10. gr.087932.108. 10.1101/gr.087932.108. PMC2665779.

    abstract

    Hox genes control many aspects of embryonic development in metazoans. Previous analyses of this gene family revealed a surprising diversity in terms of gene number and organization between various animal species. In vertebrates, Hox genes are grouped into tightly organized clusters, claimed to be devoid of repetitive sequences. Here, we report the genomic organization of the four Hox loci present in the green anole lizard and show that they have massively accumulated retrotransposons, leading to gene clusters larger in size when compared to other vertebrates. In addition, similar repeats are present in many other development-related gene-containing regions, also thought to be refractory to such repetitive elements. Transposable elements are major sources of genetic variations, including alterations of gene expression, and hence this situation, so far unique among vertebrates, may have been associated with the evolution of the spectacular realm of morphological variations in the body plans of Squamata. Finally, sequence alignments highlight some divergent evolution in highly conserved DNA regions between vertebrate Hox clusters, which may coincide with the emergence of mammalian-specific features.

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  • Unexpected diversity in the catfish Pseudancistrus brevispinis reveals dispersal routes in a Neotropical center of endemism: the Guyanas Region. Mol. Ecol. 2009 Mar;18(5):947-64. MEC4068. 10.1111/j.1365-294X.2008.04068.x.

    abstract

    Neotropical freshwater fishes have reached an unrivalled diversity, organized into several areas of endemism, yet the underlying processes are still largely unknown. The topographical and ecological characteristics of the Guyanas Region make it an ideal area of endemism in which to investigate the forces that have shaped this great diversity. This region is thought to be inhabited by species descending from Amazonian ancestors, which would have used two documented routes that, however, hardly explain the entrance of species adapted to running waters. Here, we investigate the evolutionary history of Pseudancistrus brevispinis, a catfish endemic to this region and exclusively found in running waters, thus making it an ideal model for investigating colonization routes and dispersal in such habitats. Our analyses, based on mitochondrial and nuclear markers, revealed an unexpected diversity consisting of six monophyletic lineages within P. brevispinis, showing a disjoint distribution pattern. The lineages endemic to Guyanas coastal rivers form a monophyletic group that originated via an ancestral colonization event from the Amazon basin. Evidence given favours a colonization pathway through river capture between an Amazonian tributary and the Upper Maroni River. Population genetic analyses of the most widespread species indicate that subsequent dispersal among Guyanas coastal rivers occurred principally by temporary connections between adjacent rivers during periods of lower sea level, yet instances of dispersal via interbasin river captures are not excluded. During high sea level intervals, the isolated populations would have diverged leading to the observed allopatric species. This evolutionary process is named the sea level fluctuation (SLF) hypothesis of diversification.

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  • Molecular systematic and historical biogeography of the armored Neotropical catfishes Hypoptopomatinae and Neoplecostominae (Siluriformes: Loricariidae). Mol. Phylogenet. Evol. 2008 Nov;49(2):606-17. S1055-7903(08)00415-6. 10.1016/j.ympev.2008.08.013.

    abstract

    The Neotropics possess the greatest freshwater fish diversity of the world, rendering the study of their evolutionary history extremely challenging. Loricariidae catfishes are one of the most diverse components of the Neotropical ichthyofauna and despite a long history of classification, major issues still need elucidation. Based on a nuclear gene, we present a robust phylogeny of two former loricariid subfamilies: Hypoptopomatinae and Neoplecostominae. Our results show that Neoplecostominae is nested within Hypoptopomatinae, and is the sister group to the former Otothyrini tribe. According to our results, supplemented by morphological observations, we erect two new subfamilies, the Otothyrinae and a new Hypoptopomatinae, and modify the Neoplecostominae by including the genus Pseudotocinclus. The uncovered evolutionary relationships allow a detailed analysis of their historical biogeography. We tested two Dispersal-Extinction-Cladogenesis models for inferring the distribution range evolution of the new subfamilies, and show that the model having no constrains performs better than a model constraining long-range dispersal. The Maximum Likelihood reconstructions of ancestral ranges showed a marked division between the Amazonian origin of the Hypoptopomatinae and the eastern coastal Brazil+Upper Paraná origin of the Neoplecostominae and Otothyrinae. Markedly few instances of dispersal across the border separating the Amazon basin and the Paraná-Paraguay+eastern coastal Brazil+Uruguay were reconstructed. This result is in clear contrast with the historical biogeography of many Neotropical fishes, including other Loricariidae. Part of the dispersal limitation may be explained by divergent ecological specialization: lowland rivers versus mountain streams habitats. Moreover, because most species of the new subfamilies are small, we hypothesize that body size-related effects might limit their dispersal, like predation and energetic cost to migration. Finally, morphological and anatomical features are presented that limit or, to the contrary, enhance dispersal capability in these small and fascinating catfishes.

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  • Assessing phylogenetic dependence of morphological traits using co-inertia prior to investigate character evolution in Loricariinae catfishes. Mol. Phylogenet. Evol. 2008 Mar;46(3):986-1002. S1055-7903(07)00428-9. 10.1016/j.ympev.2007.12.015.

    abstract

    With the increase of laboratory facilities, molecular phylogenies are playing a predominant role in evolutionary analyses. However, understanding the evolution of morphological traits remains essential for a comprehensive view of the evolution of a group. Here we present a new approach based on co-inertia analysis for identifying characters which variations are dependent to the phylogeny, a prerequisite for analyzing the evolution of characters. Our approach has the advantage of treating the full data set at once, including qualitative and quantitative variables. It provides a graphical output giving the contribution of each variable to the co-structure, allowing a direct discrimination among phylogenetically dependent and independent variables. We have implemented this approach in deciphering the evolution of morphological traits in a highly specialized group of Neotropical catfishes: the Loricariinae. We have first inferred a molecular phylogeny of this group based on the 12S and 16S mitochondrial genes. The resulting phylogeny indicated that the subtribe Harttiini was restricted to the single genus Harttia, and within the subtribe Loricariini, two sister subtribes were distinguished, Sturisomina (new subtribe), and Loricariina. Among Loricariina, the morphological groups Loricariichthys and Loricaria+Pseudohemiodon were confirmed. The co-inertia analysis highlighted a strong relationship between the morphological and the genetic data sets, and identified three quantitative and eight qualitative variables linked to the phylogeny. The evolution of quantitative variables was assessed using the orthogram method and showed a major punctual event in the evolution of the number of caudal-fin rays, and a more gradual pattern of evolution of the number of teeth along the phylogeny. The evolution of qualitative variables was inferred using ancestral states reconstructions and highlighted parallel patterns of evolution in characters linked to the mouth, suggesting co-evolution of the traits for adapting to divergent substrates.

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  • Life-history traits drive the evolutionary rates of mammalian coding and noncoding genomic elements. Proc. Natl. Acad. Sci. U.S.A. 2007 Dec;104(51):20443-8. 0705658104. 10.1073/pnas.0705658104. PMC2154450.

    abstract

    A comprehensive phylogenetic framework is indispensable for investigating the evolution of genomic features in mammals as a whole, and particularly in humans. Using the ENCODE sequence data, we estimated mammalian neutral evolutionary rates and selective pressures acting on conserved coding and noncoding elements. We show that neutral evolutionary rates can be explained by the generation time (GT) hypothesis. Accordingly, primates (especially humans), having longer GTs than other mammals, display slower rates of neutral evolution. The evolution of constrained elements, particularly of nonsynonymous sites, is in agreement with the expectations of the nearly neutral theory of molecular evolution. We show that rates of nonsynonymous substitutions (dN) depend on the population size of a species. The results are robust to the exclusion of hypermutable CpG prone sites. The average rate of evolution in conserved noncoding sequences (CNCs) is 1.7 times higher than in nonsynonymous sites. Despite this, CNCs evolve at similar or even lower rates than nonsynonymous sites in the majority of basal branches of the eutherian tree. This observation could be the result of an overall gradual or, alternatively, lineage-specific relaxation of CNCs. The latter hypothesis was supported by the finding that 3 of the 20 longest CNCs displayed significant relaxation of individual branches. This observation may explain why the evolution of CNCs fits the expectations of the nearly neutral theory less well than the evolution of nonsynonymous sites.

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  • Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007 Jun;447(7146):799-816. PMC2212820. NIHMS27513. 10.1038/nature05874.

    abstract

    We report the generation and analysis of functional data from multiple, diverse experiments performed on a targeted 1% of the human genome as part of the pilot phase of the ENCODE Project. These data have been further integrated and augmented by a number of evolutionary and computational analyses. Together, our results advance the collective knowledge about human genome function in several major areas. First, our studies provide convincing evidence that the genome is pervasively transcribed, such that the majority of its bases can be found in primary transcripts, including non-protein-coding transcripts, and those that extensively overlap one another. Second, systematic examination of transcriptional regulation has yielded new understanding about transcription start sites, including their relationship to specific regulatory sequences and features of chromatin accessibility and histone modification. Third, a more sophisticated view of chromatin structure has emerged, including its inter-relationship with DNA replication and transcriptional regulation. Finally, integration of these new sources of information, in particular with respect to mammalian evolution based on inter- and intra-species sequence comparisons, has yielded new mechanistic and evolutionary insights concerning the functional landscape of the human genome. Together, these studies are defining a path for pursuit of a more comprehensive characterization of human genome function.

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  • Analyses of deep mammalian sequence alignments and constraint predictions for 1% of the human genome. Genome Res. 2007 Jun;17(6):760-74. 17/6/760. 10.1101/gr.6034307. PMC1891336.

    abstract

    A key component of the ongoing ENCODE project involves rigorous comparative sequence analyses for the initially targeted 1% of the human genome. Here, we present orthologous sequence generation, alignment, and evolutionary constraint analyses of 23 mammalian species for all ENCODE targets. Alignments were generated using four different methods; comparisons of these methods reveal large-scale consistency but substantial differences in terms of small genomic rearrangements, sensitivity (sequence coverage), and specificity (alignment accuracy). We describe the quantitative and qualitative trade-offs concomitant with alignment method choice and the levels of technical error that need to be accounted for in applications that require multisequence alignments. Using the generated alignments, we identified constrained regions using three different methods. While the different constraint-detecting methods are in general agreement, there are important discrepancies relating to both the underlying alignments and the specific algorithms. However, by integrating the results across the alignments and constraint-detecting methods, we produced constraint annotations that were found to be robust based on multiple independent measures. Analyses of these annotations illustrate that most classes of experimentally annotated functional elements are enriched for constrained sequences; however, large portions of each class (with the exception of protein-coding sequences) do not overlap constrained regions. The latter elements might not be under primary sequence constraint, might not be constrained across all mammals, or might have expendable molecular functions. Conversely, 40% of the constrained sequences do not overlap any of the functional elements that have been experimentally identified. Together, these findings demonstrate and quantify how many genomic functional elements await basic molecular characterization.

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  • Divergent evolution among teleost V1r receptor genes. PLoS ONE 2007 ;2(4):e379. 10.1371/journal.pone.0000379. PMC1849887.

    abstract

    The survival of vertebrate species is dependent on the ability of individuals to adequately interact with each other, a function often mediated by the olfactory system. Diverse olfactory receptor repertoires are used by this system to recognize chemicals. Among these receptors, the V1rs, encoded by a very large gene family in most mammals, are able to detect pheromones. Teleosts, which also express V1r receptors, possess a very limited V1r repertoire. Here, taking advantage of the possibility to unequivocally identify V1r orthologs in teleosts, we analyzed the olfactory expression and evolutionary constraints of a pair of clustered fish V1r receptor genes, V1r1 and V1r2. Orthologs of the two genes were found in zebrafish, medaka, and threespine stickleback, but a single representative was observed in tetraodontidae species. Analysis of V1r1 and V1r2 sequences from 12 different euteleost species indicate different evolutionary rates between the two paralogous genes, leading to a highly conserved V1r2 gene and a V1r1 gene under more relaxed selective constraint. Moreover, positively-selected sites were detected in specific branches of the V1r1 clade. Our results suggest a conserved agonist specificity of the V1R2 receptor between euteleost species, its loss in the tetraodontidae lineage, and the acquisition of different chemosensory characteristics for the V1R1 receptor.

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  • Early history of mammals is elucidated with the ENCODE multiple species sequencing data. PLoS Genet. 2007 Jan;3(1):e2. 06-PLGE-RA-0299R2. 10.1371/journal.pgen.0030002. PMC1761045.

    abstract

    Understanding the early evolution of placental mammals is one of the most challenging issues in mammalian phylogeny. Here, we addressed this question by using the sequence data of the ENCODE consortium, which include 1% of mammalian genomes in 18 species belonging to all main mammalian lineages. Phylogenetic reconstructions based on an unprecedented amount of coding sequences taken from 218 genes resulted in a highly supported tree placing the root of Placentalia between Afrotheria and Exafroplacentalia (Afrotheria hypothesis). This topology was validated by the phylogenetic analysis of a new class of genomic phylogenetic markers, the conserved noncoding sequences. Applying the tests of alternative topologies on the coding sequence dataset resulted in the rejection of the Atlantogenata hypothesis (Xenarthra grouping with Afrotheria), while this test rejected the second alternative scenario, the Epitheria hypothesis (Xenarthra at the base), when using the noncoding sequence dataset. Thus, the two datasets support the Afrotheria hypothesis; however, none can reject both of the remaining topological alternatives.

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  • Conserved domains control heterochromatin localization and silencing properties of SU(VAR)3-7. Chromosoma. 2006 Apr;115(2):139-50. Epub 2006 Feb 7.

    abstract

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  • Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Mol. Phylogenet. Evol. 2006 Jan;38(1):20-30. S1055-7903(05)00171-5. 10.1016/j.ympev.2005.04.028.

    abstract

    Symbiotic dinoflagellates belonging to the genus Symbiodinium are found in association with a wide variety of shallow-water invertebrates and protists dwelling in tropical and subtropical coral-reef ecosystems. Molecular phylogeny of Symbiodinium, initially inferred using nuclear ribosomal genes, was recently confirmed by studies of chloroplastic and mitochondrial genes, but with limited taxon sampling and low resolution. Here, we present the first complete view of Symbiodinium phylogeny based on concatenated partial sequences of chloroplast 23S-rDNA (cp23S) and nuclear 28S-rDNA (nr28S) genes, including all known Symbiodinium lineages. Our data produced a well resolved phylogenetic tree and provide a strong statistical support for the eight distinctive clades (A-H) that form the major taxa of Symbiodinium. The relative-rate tests did not show particularly high differences between lineages and both analysed markers. However, maximum likelihood ratio tests rejected a global molecular clock. Therefore, we applied a relaxed molecular clock method to infer the divergence times of all extant lineages of Symbiodinium, calibrating its phylogenetic tree with the fossil record of soritid foraminifera. Our analysis suggests that Symbiodinium originated in early Eocene, and that the majority of extant lineages diversified since mid-Miocene, about 15 million years ago.

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  • Recombination explains isochores in mammalian genomes. Trends Genet. 2003 Mar;19(3):128-30. S0168-9525(03)00021-0. 10.1016/S0168-9525(03)00021-0.

    abstract

    The mouse Fxy gene was translocated into the highly recombining pseudoautosomal region comparatively recently in evolutionary terms. This event resulted in a rapid increase of GC content. We investigated the consequences of the translocation further by sequencing exons and introns of Fxy in various rodent species. We found that the DNA fragment newly located in a highly recombining context has acquired every property of a GC-rich isochore, namely increased GC content (especially at the third codon positions of exons), shorter introns and high density of minisatellites. These results strongly suggest that recombination is the primary determinant of the isochore organization of mammalian genomes.

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