About 6 % of an estimated total of 240 000 species of angiosperms are dioecious. The main precurs... more About 6 % of an estimated total of 240 000 species of angiosperms are dioecious. The main precursors of this sexual system are thought to be monoecy and gynodioecy. A previous angiosperm-wide study revealed that many dioecious species have evolved through the monoecy pathway; some case studies and a large body of theoretical research also provide evidence in support of the gynodioecy pathway. If plants have evolved through the gynodioecy pathway, gynodioecious and dioecious species should co-occur in the same genera. However, to date, no large-scale analysis has been conducted to determine the prevalence of the gynodioecy pathway in angiosperms. In this study, this gap in knowledge was addressed by performing an angiosperm-wide survey in order to test for co-occurrence as evidence of the gynodioecy pathway. Data from different sources were compiled to obtain (to our knowledge) the largest dataset on gynodioecy available, with 275 genera that include at least one gynodioecious specie...
Rates of recombination can vary among genomic regions in eukaryotes, and this is believed to have... more Rates of recombination can vary among genomic regions in eukaryotes, and this is believed to have major effects on their genome organization in terms of base composition, DNA repeat density, intron size, evolutionary rates and gene order. In highly self-fertilizing species such as Arabidopsis thaliana, however, heterozygosity is expected to be strongly reduced and recombination will be much less effective, so that its influence on genome organization should be greatly reduced. Here we investigated theoretically the joint effects of recombination and self-fertilization on base composition, and tested the predictions with genomic data from the complete A. thaliana genome. We show that, in this species, both codon-usage bias and GC content do not correlate with the local rates of crossing over, in agreement with our theoretical results. We conclude that levels of inbreeding modulate the effect of recombination on base composition, and possibly other genomic features (for example, trans...
In many unicellular organisms, invertebrates, and plants, synonymous codon usage biases result fr... more In many unicellular organisms, invertebrates, and plants, synonymous codon usage biases result from a coadaptation between codon usage and tRNAs abundance to optimize the efficiency of protein synthesis. However, it remains unclear whether natural selection acts at the level of the speed or the accuracy of mRNAs translation. Here we show that codon usage can improve the fidelity of protein synthesis in multicellular species. As predicted by the model of selection for translational accuracy, we find that the frequency of codons optimal for translation is significantly higher at codons encoding for conserved amino acids than at codons encoding for nonconserved amino acids in 548 genes compared between Caenorhabditis elegans and Homo sapiens. Although this model predicts that codon bias correlates positively with gene length, a negative correlation between codon bias and gene length has been observed in eukaryotes. This suggests that selection for fidelity of protein synthesis is not t...
We analyzed the distribution of transposable elements (TEs: transposons, LTR retrotransposons, an... more We analyzed the distribution of transposable elements (TEs: transposons, LTR retrotransposons, and non-LTR retrotransposons) in the chromosomes of the nematode Caenorhabditis elegans. The density of transposons (DNA-based elements) along the chromosomes was found to be positively correlated with recombination rate, but this relationship was not observed for LTR or non-LTR retrotransposons (RNA-based elements). Gene (coding region) density is higher in regions of low recombination rate. However, the lower TE density in these regions is not due to the counterselection of TE insertions within exons since the same positive correlation between TE density and recombination rate was found in noncoding regions (both in introns and intergenic DNA). These data are not compatible with a global model of selection acting against TE insertions, for which an accumulation of elements in regions of reduced recombination is expected. We also found no evidence for a stronger selection against TE inser...
To identify the factors (selective or mutational) that affect the distribution of transposable el... more To identify the factors (selective or mutational) that affect the distribution of transposable elements (TEs) within a genome, it is necessary to compare the pattern of newly arising element insertions to the pattern of element insertions that have been fixed in a population. To do this, we analyzed the distribution of recent mutant insertions of the Tc1, Tc3, and Tc5 elements in a mut-7 background of the nematode Caenorhabditis elegans and compared it to the distribution of element insertions (presumably fixed) within the sequenced genome. Tc1 elements preferentially insert in regions with high recombination rates, whereas Tc3 and Tc5 do not. Although Tc1 and Tc3 both insert in TA dinucleotides, there is no clear relationship between the frequency of insertions and the TA dinucleotide density. There is a strong selection against TE insertions within coding regions: the probability that a TE will be fixed is at least 31 times lower in coding regions than in noncoding regions. Contrary to the prediction of theoretical models, we found that the selective pressure against TE insertions does not increase with the recombination rate. These findings indicate that the distribution of these three transposon families in the genome of C. elegans is determined essentially by just two factors: the pattern of insertions, which is a characteristic of each family, and the selection against insertions within coding regions.
Proceedings of the National Academy of Sciences, 2001
Understanding the factors responsible for variations in mutation patterns and selection efficacy ... more Understanding the factors responsible for variations in mutation patterns and selection efficacy along chromosomes is a prerequisite for deciphering genome sequences. Population genetics models predict a positive correlation between the efficacy of selection at a given locus and the local rate of recombination because of Hill-Robertson effects. Codon usage is considered one of the most striking examples that support this prediction at the molecular level. In a wide range of species including Caenorhabditis elegans and Drosophila melanogaster, codon usage is essentially shaped by selection acting for translational efficiency. Codon usage bias correlates positively with recombination rate in Drosophila, apparently supporting the hypothesis that selection on codon usage is improved by recombination. Here we present an exhaustive analysis of codon usage in C. elegans and D. melanogaster complete genomes. We show that in both genomes there is a positive correlation between recombination rate and the frequency of optimal codons. However, we demonstrate that in both species, this effect is due to a mutational bias toward G and C bases in regions of high recombination rate, possibly as a direct consequence of the recombination process. The correlation between codon usage bias and recombination rate in these species appears to be essentially determined by recombination-dependent mutational patterns, rather than selective effects. This result highlights that it is necessary to take into account the mutagenic effect of recombination to understand the evolutionary role and impact of recombination.
According to population genetics models, genomic regions with lower crossing-over rates are expec... more According to population genetics models, genomic regions with lower crossing-over rates are expected to experience less effective selection because of Hill-Robertson interference (HRi). The effect of genetic linkage is thought to be particularly important for a selection of weak intensity such as selection affecting codon usage. Consistent with this model, codon bias correlates positively with recombination rate in Drosophila melanogaster and Caenorhabditis elegans. However, in these species, the G+C content of both noncoding DNA and synonymous sites correlates positively with recombination, which suggests that mutation patterns and recombination are associated. To remove this effect of mutation patterns on codon bias, we used the synonymous sites of lowly expressed genes that are expected to be effectively neutral sites. We measured the differences between codon biases of highly expressed genes and their lowly expressed neighbors. In D. melanogaster we find that HRi weakly reduces selection on codon usage of genes located in regions of very low recombination; but these genes only comprise 4% of the total. In C. elegans we do not find any evidence for the effect of recombination on selection for codon bias. Computer simulations indicate that HRi poorly enhances codon bias if the local recombination rate is greater than the mutation rate. This prediction of the model is consistent with our data and with the current estimate of the mutation rate in D. melanogaster. The case of C. elegans, which is highly self-fertilizing, is discussed. Our results suggest that HRi is a minor determinant of variations in codon bias across the genome.
ABSTRACT In angiosperms, dioecious clades tend to have fewer species than their nondioecious sist... more ABSTRACT In angiosperms, dioecious clades tend to have fewer species than their nondioecious sister clades. This departure from the expected equal species richness in the standard sister clade test has been interpreted as implying that dioecious clades diversify less and has initiated a series of studies suggesting that dioecy might be an 'evolutionary dead end‘. However, two of us recently showed that the ‘equal species richness‘ null hypothesis is not valid in the case of derived char acters, such as dioecy, and proposed a new test for sister clade comparisons; preliminary results, using a data set available in the litterature, indicated that dioecious clades migth diversify more than expected. However, it is crucial for this new test to distinguish between ancestral and derived cases of dioecy, a criterion that was not taken into account in the available data set. Here, we present a new data set that was obtained by searching the phylogenetic literature on more than 600 completely dioecious angiosperm genera and identifying 115 sister clade pairs for which dioecy is likely to be derived (including > 50% of the dioecious species). Applying the new sister clade test to this new dataset, we confirm the preliminary result that dioecy is associated with an increased diversification rate, a result that does not support the idea that dioecy is an evolutionary dead end in angiosperms. The traits usually associated with dioecy, that is, an arborescent growth form, abiotic pollination, fleshy fruits or a tropical distribution, do not influence the diversification rate. Rather than a low diversification rate, the observed species richness patterns of dioecious clades seem to be better explained by a low transition rate to dioecy and frequent losses.
Recombination is thought to have various evolutionary effects on genome evolution. In this study,... more Recombination is thought to have various evolutionary effects on genome evolution. In this study, we investigated the relationship between the base composition and recombination rate in the Drosophila melanogaster genome. Because of a current debate about the accuracy of the estimates of recombination rate in Drosophila, we used eight different measures of recombination rate from recent work. We confirmed that the G + C content of large introns and flanking regions is positively correlated with recombination rate, suggesting that recombination has a neutral effect on base composition in Drosophila. We also confirmed that this neutral effect of recombination is the main determinant of the correlation between synonymous codon usage bias and recombination rate in Drosophila.
Mutual interference among linked genetic sites subject to selection may reduce the level of adapt... more Mutual interference among linked genetic sites subject to selection may reduce the level of adaptation. A recent study detected this effect using data on protein sequence evolution and codon usage in Drosophila.
Bacterial genomes show substantial variations in size. The smallest bacterial genomes are those o... more Bacterial genomes show substantial variations in size. The smallest bacterial genomes are those of endocellular symbionts of eukaryotic hosts, which have undergone massive genome reduction and show patterns that are consistent with the degenerative processes that are predicted to occur in species with small effective population sizes. However, similar genome reduction is found in some free-living marine cyanobacteria that are characterized by extremely large populations. In this Opinion article, we discuss the different hypotheses that have been proposed to account for this reductive genome evolution at both ends of the bacterial population size spectrum.
International Journal of Evolutionary Biology, 2012
Comparative genome analysis has allowed the identification of various mechanisms involved in gene... more Comparative genome analysis has allowed the identification of various mechanisms involved in gene birth. However, understanding the evolutionary forces driving new gene origination still represents a major challenge. In particular, an intriguing and not yet fully understood trend has emerged from the study of new genes: many of them show a testis-specific expression pattern, which has remained poorly understood. Here we review the case of such a new gene, which involves a telomere-capping gene family in Drosophila. hiphop and its testis-specific paralog K81 are critical for the protection of chromosome ends in somatic cells and male gametes, respectively. Two independent functional studies recently proposed that these genes evolved under a reproductive-subfunctionalization regime. The 2011 release of new Drosophila genome sequences from the melanogaster group of species allowed us to deepen our phylogenetic analysis of the hiphop/K81 family. This work reveals an unsuspected dynamic of gene birth and death within the group, with recurrent duplication events through retroposition mechanisms. Finally, we discuss the plausibility of different evolutionary scenarios that could explain the diversification of this gene family.
About 6 % of an estimated total of 240 000 species of angiosperms are dioecious. The main precurs... more About 6 % of an estimated total of 240 000 species of angiosperms are dioecious. The main precursors of this sexual system are thought to be monoecy and gynodioecy. A previous angiosperm-wide study revealed that many dioecious species have evolved through the monoecy pathway; some case studies and a large body of theoretical research also provide evidence in support of the gynodioecy pathway. If plants have evolved through the gynodioecy pathway, gynodioecious and dioecious species should co-occur in the same genera. However, to date, no large-scale analysis has been conducted to determine the prevalence of the gynodioecy pathway in angiosperms. In this study, this gap in knowledge was addressed by performing an angiosperm-wide survey in order to test for co-occurrence as evidence of the gynodioecy pathway. Data from different sources were compiled to obtain (to our knowledge) the largest dataset on gynodioecy available, with 275 genera that include at least one gynodioecious specie...
Rates of recombination can vary among genomic regions in eukaryotes, and this is believed to have... more Rates of recombination can vary among genomic regions in eukaryotes, and this is believed to have major effects on their genome organization in terms of base composition, DNA repeat density, intron size, evolutionary rates and gene order. In highly self-fertilizing species such as Arabidopsis thaliana, however, heterozygosity is expected to be strongly reduced and recombination will be much less effective, so that its influence on genome organization should be greatly reduced. Here we investigated theoretically the joint effects of recombination and self-fertilization on base composition, and tested the predictions with genomic data from the complete A. thaliana genome. We show that, in this species, both codon-usage bias and GC content do not correlate with the local rates of crossing over, in agreement with our theoretical results. We conclude that levels of inbreeding modulate the effect of recombination on base composition, and possibly other genomic features (for example, trans...
In many unicellular organisms, invertebrates, and plants, synonymous codon usage biases result fr... more In many unicellular organisms, invertebrates, and plants, synonymous codon usage biases result from a coadaptation between codon usage and tRNAs abundance to optimize the efficiency of protein synthesis. However, it remains unclear whether natural selection acts at the level of the speed or the accuracy of mRNAs translation. Here we show that codon usage can improve the fidelity of protein synthesis in multicellular species. As predicted by the model of selection for translational accuracy, we find that the frequency of codons optimal for translation is significantly higher at codons encoding for conserved amino acids than at codons encoding for nonconserved amino acids in 548 genes compared between Caenorhabditis elegans and Homo sapiens. Although this model predicts that codon bias correlates positively with gene length, a negative correlation between codon bias and gene length has been observed in eukaryotes. This suggests that selection for fidelity of protein synthesis is not t...
We analyzed the distribution of transposable elements (TEs: transposons, LTR retrotransposons, an... more We analyzed the distribution of transposable elements (TEs: transposons, LTR retrotransposons, and non-LTR retrotransposons) in the chromosomes of the nematode Caenorhabditis elegans. The density of transposons (DNA-based elements) along the chromosomes was found to be positively correlated with recombination rate, but this relationship was not observed for LTR or non-LTR retrotransposons (RNA-based elements). Gene (coding region) density is higher in regions of low recombination rate. However, the lower TE density in these regions is not due to the counterselection of TE insertions within exons since the same positive correlation between TE density and recombination rate was found in noncoding regions (both in introns and intergenic DNA). These data are not compatible with a global model of selection acting against TE insertions, for which an accumulation of elements in regions of reduced recombination is expected. We also found no evidence for a stronger selection against TE inser...
To identify the factors (selective or mutational) that affect the distribution of transposable el... more To identify the factors (selective or mutational) that affect the distribution of transposable elements (TEs) within a genome, it is necessary to compare the pattern of newly arising element insertions to the pattern of element insertions that have been fixed in a population. To do this, we analyzed the distribution of recent mutant insertions of the Tc1, Tc3, and Tc5 elements in a mut-7 background of the nematode Caenorhabditis elegans and compared it to the distribution of element insertions (presumably fixed) within the sequenced genome. Tc1 elements preferentially insert in regions with high recombination rates, whereas Tc3 and Tc5 do not. Although Tc1 and Tc3 both insert in TA dinucleotides, there is no clear relationship between the frequency of insertions and the TA dinucleotide density. There is a strong selection against TE insertions within coding regions: the probability that a TE will be fixed is at least 31 times lower in coding regions than in noncoding regions. Contrary to the prediction of theoretical models, we found that the selective pressure against TE insertions does not increase with the recombination rate. These findings indicate that the distribution of these three transposon families in the genome of C. elegans is determined essentially by just two factors: the pattern of insertions, which is a characteristic of each family, and the selection against insertions within coding regions.
Proceedings of the National Academy of Sciences, 2001
Understanding the factors responsible for variations in mutation patterns and selection efficacy ... more Understanding the factors responsible for variations in mutation patterns and selection efficacy along chromosomes is a prerequisite for deciphering genome sequences. Population genetics models predict a positive correlation between the efficacy of selection at a given locus and the local rate of recombination because of Hill-Robertson effects. Codon usage is considered one of the most striking examples that support this prediction at the molecular level. In a wide range of species including Caenorhabditis elegans and Drosophila melanogaster, codon usage is essentially shaped by selection acting for translational efficiency. Codon usage bias correlates positively with recombination rate in Drosophila, apparently supporting the hypothesis that selection on codon usage is improved by recombination. Here we present an exhaustive analysis of codon usage in C. elegans and D. melanogaster complete genomes. We show that in both genomes there is a positive correlation between recombination rate and the frequency of optimal codons. However, we demonstrate that in both species, this effect is due to a mutational bias toward G and C bases in regions of high recombination rate, possibly as a direct consequence of the recombination process. The correlation between codon usage bias and recombination rate in these species appears to be essentially determined by recombination-dependent mutational patterns, rather than selective effects. This result highlights that it is necessary to take into account the mutagenic effect of recombination to understand the evolutionary role and impact of recombination.
According to population genetics models, genomic regions with lower crossing-over rates are expec... more According to population genetics models, genomic regions with lower crossing-over rates are expected to experience less effective selection because of Hill-Robertson interference (HRi). The effect of genetic linkage is thought to be particularly important for a selection of weak intensity such as selection affecting codon usage. Consistent with this model, codon bias correlates positively with recombination rate in Drosophila melanogaster and Caenorhabditis elegans. However, in these species, the G+C content of both noncoding DNA and synonymous sites correlates positively with recombination, which suggests that mutation patterns and recombination are associated. To remove this effect of mutation patterns on codon bias, we used the synonymous sites of lowly expressed genes that are expected to be effectively neutral sites. We measured the differences between codon biases of highly expressed genes and their lowly expressed neighbors. In D. melanogaster we find that HRi weakly reduces selection on codon usage of genes located in regions of very low recombination; but these genes only comprise 4% of the total. In C. elegans we do not find any evidence for the effect of recombination on selection for codon bias. Computer simulations indicate that HRi poorly enhances codon bias if the local recombination rate is greater than the mutation rate. This prediction of the model is consistent with our data and with the current estimate of the mutation rate in D. melanogaster. The case of C. elegans, which is highly self-fertilizing, is discussed. Our results suggest that HRi is a minor determinant of variations in codon bias across the genome.
ABSTRACT In angiosperms, dioecious clades tend to have fewer species than their nondioecious sist... more ABSTRACT In angiosperms, dioecious clades tend to have fewer species than their nondioecious sister clades. This departure from the expected equal species richness in the standard sister clade test has been interpreted as implying that dioecious clades diversify less and has initiated a series of studies suggesting that dioecy might be an 'evolutionary dead end‘. However, two of us recently showed that the ‘equal species richness‘ null hypothesis is not valid in the case of derived char acters, such as dioecy, and proposed a new test for sister clade comparisons; preliminary results, using a data set available in the litterature, indicated that dioecious clades migth diversify more than expected. However, it is crucial for this new test to distinguish between ancestral and derived cases of dioecy, a criterion that was not taken into account in the available data set. Here, we present a new data set that was obtained by searching the phylogenetic literature on more than 600 completely dioecious angiosperm genera and identifying 115 sister clade pairs for which dioecy is likely to be derived (including > 50% of the dioecious species). Applying the new sister clade test to this new dataset, we confirm the preliminary result that dioecy is associated with an increased diversification rate, a result that does not support the idea that dioecy is an evolutionary dead end in angiosperms. The traits usually associated with dioecy, that is, an arborescent growth form, abiotic pollination, fleshy fruits or a tropical distribution, do not influence the diversification rate. Rather than a low diversification rate, the observed species richness patterns of dioecious clades seem to be better explained by a low transition rate to dioecy and frequent losses.
Recombination is thought to have various evolutionary effects on genome evolution. In this study,... more Recombination is thought to have various evolutionary effects on genome evolution. In this study, we investigated the relationship between the base composition and recombination rate in the Drosophila melanogaster genome. Because of a current debate about the accuracy of the estimates of recombination rate in Drosophila, we used eight different measures of recombination rate from recent work. We confirmed that the G + C content of large introns and flanking regions is positively correlated with recombination rate, suggesting that recombination has a neutral effect on base composition in Drosophila. We also confirmed that this neutral effect of recombination is the main determinant of the correlation between synonymous codon usage bias and recombination rate in Drosophila.
Mutual interference among linked genetic sites subject to selection may reduce the level of adapt... more Mutual interference among linked genetic sites subject to selection may reduce the level of adaptation. A recent study detected this effect using data on protein sequence evolution and codon usage in Drosophila.
Bacterial genomes show substantial variations in size. The smallest bacterial genomes are those o... more Bacterial genomes show substantial variations in size. The smallest bacterial genomes are those of endocellular symbionts of eukaryotic hosts, which have undergone massive genome reduction and show patterns that are consistent with the degenerative processes that are predicted to occur in species with small effective population sizes. However, similar genome reduction is found in some free-living marine cyanobacteria that are characterized by extremely large populations. In this Opinion article, we discuss the different hypotheses that have been proposed to account for this reductive genome evolution at both ends of the bacterial population size spectrum.
International Journal of Evolutionary Biology, 2012
Comparative genome analysis has allowed the identification of various mechanisms involved in gene... more Comparative genome analysis has allowed the identification of various mechanisms involved in gene birth. However, understanding the evolutionary forces driving new gene origination still represents a major challenge. In particular, an intriguing and not yet fully understood trend has emerged from the study of new genes: many of them show a testis-specific expression pattern, which has remained poorly understood. Here we review the case of such a new gene, which involves a telomere-capping gene family in Drosophila. hiphop and its testis-specific paralog K81 are critical for the protection of chromosome ends in somatic cells and male gametes, respectively. Two independent functional studies recently proposed that these genes evolved under a reproductive-subfunctionalization regime. The 2011 release of new Drosophila genome sequences from the melanogaster group of species allowed us to deepen our phylogenetic analysis of the hiphop/K81 family. This work reveals an unsuspected dynamic of gene birth and death within the group, with recurrent duplication events through retroposition mechanisms. Finally, we discuss the plausibility of different evolutionary scenarios that could explain the diversification of this gene family.
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Papers by Gabriel Marais