BMC Evolutionary Biology - Latest Articles

Convergent evolution, habitat shifts and variable diversification rates in the ovenbird-woodcreeper family (Furnariidae)

Martin Irestedt — 2009-11-21T00:00:00Z

Background: The Neotropical ovenbird-woodcreeper family (Furnariidae) is an avian group characterized by exceptionally diverse ecomorphological adaptations. For instance, members of the family are known to construct nests of a remarkable variety. This offers a unique opportunity to examine whether changes in nest design, accompanied by expansions into new habitats, facilitates diversification. We present a multi-gene phylogeny and age estimates for the ovenbird-woodcreeper family and use these results to estimate the degree of convergent evolution in both phenotype and habitat utilisation. Furthermore, we discuss whether variation in species richness among ovenbird clades could be explained by differences in clade-specific diversification rates, and whether these rates differ among lineages with different nesting habits. In addition, the systematic positions of some enigmatic ovenbird taxa and the postulated monophyly of some species-rich genera are evaluated. Results: The phylogenetic results reveal new examples of convergent evolution and show that ovenbirds have independently colonized open habitats at least six times. The calculated age estimates suggest that the ovenbird-woodcreeper family started to diverge at ca 33 Mya, and that the timing of habitat shifts into open environments may be correlated with the aridification of South America during the last 15 My. The results also show that observed large differences in species richness among clades can be explained by a substantial variation in net diversification rates. The synallaxines, which generally are adapted to dry habitats and build exposed vegetative nests, had the highest diversification rate of all major furnariid clades. Conclusions: Several key features may have played an important role for the radiation and evolution of convergent phenotypes in the ovenbird-woodcreeper family. Our results suggest that changes in nest building strategy and adaptation to novel habitats may have played an important role in a diversification that included multiple radiations into more open and bushy environments. The synallaxines were found to have had a particularly high diversification rate, which may be explained by their ability to build exposed vegetative nests and thus to expand into a variety of novel habitats that emerged during a period of cooling and aridification in South America.

Diversification of the cullin family

Ignacio Marin — 2009-11-19T00:00:00Z

Background: Cullins are proteins involved in ubiquitination through their participation in multisubunit ubiquitin ligase complexes. In this study, I use comparative genomic data to establish the pattern of emergence and diversification of cullins in eukaryotes. Results: The available data indicate that there were three cullin genes before the unikont/bikont split, which I have called Cul-alpha, Cul-beta and Cul-gamma. Fungal species have quite strictly conserved these three ancestral genes, with only occasional lineage-specific duplications. On the contrary, several additional genes appeared in the animal or plant lineages. For example, the human genes Cul1, Cul2, Cul5, Cul7 and Parc all derive from the ancestral Cul-alpha gene. These results, together with the available functional data, suggest that three different types of ubiquitin ligase cullin-containing complexes were already present in early eukaryotic evolution: 1) SCF-like complexes with Cul-alpha proteins; 2) Cul-beta/BTB complexes; and, 3) Complexes containing Cul-gamma and DDB1-like proteins. Complexes containing elongins have arisen more recently and perhaps twice independently in animals and fungi. Conclusions: Most of the known types of cullin-containing ubiquitin ligase complexes are ancient. The available data suggest that, since the origin of eukaryotes, complex diversity has been mostly generated by combining closely related subunits, while radical innovations, giving rise to novel types of complexes, have been scarce. However, several protist groups not examined so far contain highly divergent cullins, indicating that additional types of complexes may exist.

Phylogenomic analysis of the cystatin superfamily in eukaryotes and prokaryotes

Dusan Kordis — 2009-11-18T00:00:00Z

Background: The cystatin superfamily comprises cysteine protease inhibitors that play key regulatory roles in protein degradation processes. Although they have been the subject of many studies, little is known about their genesis, evolution and functional diversification. Our aim has been to obtain a comprehensive insight into their origin, distribution, diversity, evolution and classification in Eukaryota, Bacteria and Archaea. Results: We have identified in silico the full complement of the cystatin superfamily in more than 2100 prokaryotic and eukaryotic genomes. The analysis of numerous eukaryotic genomes has provided strong evidence for the emergence of this superfamily in the ancestor of eukaryotes. The progenitor of this superfamily was most probably intracellular and lacked a signal peptide and disulfide bridges, much like the extant Giardia cystatin. A primordial gene duplication produced two ancestral eukaryotic lineages, cystatins and stefins. While stefins remain encoded by a single or a small number of genes throughout the eukaryotes, the cystatins have undergone a more complex and dynamic evolution through numerous gene and domain duplications. In the cystatin superfamily we discovered twenty vertebrate-specific and three angiosperm-specific orthologous families, indicating that functional diversification has occurred only in multicellular eukaryotes. In vertebrate orthologous families, the prevailing trends were loss of the ancestral inhibitory activity and acquisition of novel functions in innate immunity. Bacterial cystatins and stefins may be emergency inhibitors that enable survival of bacteria in the host, defending them from the host's proteolytic activity. Conclusions: This study challenges the current view on the classification, origin and evolution of the cystatin superfamily and provides valuable insights into their functional diversification. The findings of this comprehensive study provide guides for future structural and evolutionary studies of the cystatin superfamily as well as of other protease inhibitors and proteases.

Ribosomal protein L10 is encoded in the mitochondrial genome of many land plants and green algae

Jeffrey Mower — 2009-11-16T00:00:00Z

Background: The mitochondrial genomes of plants generally encode 30-40 identified protein-coding genes and a large number of lineage-specific ORFs. The lack of wide conservation for most ORFs suggests they are unlikely to be functional. However, an ORF, termed orf-bryo1, was recently found to be conserved among bryophytes suggesting that it might indeed encode a functional mitochondrial protein. Results: From a broad survey of land plants, we have found that the orf-bryo1 gene is also conserved in the mitochondria of vascular plants and charophycean green algae. This gene is actively transcribed and RNA edited in many flowering plants. Comparative sequence analysis and distribution of editing suggests that it encodes ribosomal protein L10 of the large subunit of the ribosome. In several lineages, such as crucifers and grasses, where the rpl10 gene has been lost from the mitochondrion, we suggest that a copy of the nucleus-encoded chloroplast-derived rpl10 gene may serve as a functional replacement. Conclusion: Despite the fact that there are now over 20 mitochondrial genome sequences for land plants and green algae, this gene has remained unidentified and largely undetected until now because of the unlikely coincidence that most of the earlier sequences were from the few lineages that lack the intact gene. These results illustrate the power of comparative sequencing to identify novel genomic features.

Genome wide evolutionary analyses reveal serotype specific patterns of positive selection in selected Salmonella serotypes

Yesim Soyer — 2009-11-14T00:00:00Z

Background: The bacterium Salmonella enterica includes a diversity of serotypes that cause disease in humans and different animal species. Some Salmonella serotypes show a broad host range, some are host restricted and exclusively associated with one particular host, and some are associated with one particular host species, but able to cause disease in other host species and are thus considered "host adapted". Five Salmonella genome sequences, representing a broad host range serotype (Typhimurium), two host restricted serotypes (Typhi [two genomes] and Paratyphi) and one host adapted serotype (Choleraesuis) were used to identify core genome genes that show evidence for recombination and positive selection. Results: Overall, 3323 orthologous genes were identified in all 5 Salmonella genomes analyzed. Use of four different methods to assess homologous recombination identified 270 genes that showed evidence for recombination with at least one of these methods (false discovery rate [FDR] <10%). After exclusion of genes with evidence for recombination, site and branch specific models identified 41 genes as showing evidence for positive selection (FDR <20%), including a number of genes with confirmed or likely roles in virulence and ompC, a gene encoding an outer membrane protein, which has also been found to be under positive selection in other bacteria. A total of 8, 16, 7, and 5 genes showed evidence for positive selection in Choleraesuis, Typhi, Typhimurium, and Paratyphi branch analyses, respectively. Sequencing and evolutionary analyses of four genes in an additional 42 isolates representing 23 serotypes confirmed branch specific positive selection and recombination patterns. Conclusion: Our data show that, among the four serotypes analyzed, (i) less than 10% of Salmonella genes in the core genome show evidence for homologous recombination, (ii) a number of Salmonella genes are under positive selection, including genes that appear to contribute to virulence, and (iii) branch specific positive selection contributes to the evolution of host restricted Salmonella serotypes.

Rapid radiation in spiny lobsters (Palinurus spp) as revealed by classic and ABC methods using mtDNA and microsatellite data

Ferran Palero — 2009-11-09T00:00:00Z

Background: Molecular tools may help to uncover closely related and still diverging species from a wide variety of taxa and provide insight into the mechanisms, pace and geography of marine speciation. There is a certain controversy on the phylogeography and speciation modes of species-groups with an Eastern Atlantic-Western Indian Ocean distribution, with previous studies suggesting that older events (Miocene) and/or more recent (Pleistocene) oceanographic processes could have influenced the phylogeny of marine taxa. The spiny lobster genus Palinurus allows for testing among speciation hypotheses, since it has a particular distribution with two groups of three species each in the Northeastern Atlantic (P. elephas, P. mauritanicus and P. charlestoni) and Southeastern Atlantic and Southwestern Indian Oceans (P. gilchristi, P. delagoae and P. barbarae). In the present study, we obtain a more complete understanding of the phylogenetic relationships among these species through a combined dataset with both nuclear and mitochondrial markers, by testing alternative hypotheses on both the mutation rate and tree topology under the recently developed approximate Bayesian computation (ABC) methods. Results: Our analyses support a North-to-South speciation pattern in Palinurus with all the South-African species forming a monophyletic clade nested within the Northern Hemisphere species. Coalescent-based ABC methods allowed us to reject the previously proposed hypothesis of a Middle Miocene speciation event related with the closure of the Tethyan Seaway. Instead, divergence times obtained for Palinurus species using the combined mtDNA-microsatellite dataset and standard mutation rates for mtDNA agree with known glaciation-related processes occurring during the last 2 my. Conclusion: The Palinurus speciation pattern is a typical example of a series of rapid speciation events occurring within a group, with very short branches separating different species. Our results support the hypothesis that recent climate change-related oceanographic processes have influenced the phylogeny of marine taxa, with most Palinurus species originating during the last two million years. The present study highlights the value of new coalescent-based statistical methods such as ABC for testing different speciation hypotheses using molecular data.

Asymmetric introgression between sympatric molestus and pipiens forms of Culex pipiens (Diptera: Culicidae) in the Comporta region, Portugal

Bruno Gomes — 2009-11-06T00:00:00Z

Background: Culex pipiens L. is the most widespread mosquito vector in temperate regions. This species consists of two forms, denoted molestus and pipiens, that exhibit important behavioural and physiological differences. The evolutionary relationships and taxonomic status of these forms remain unclear. In northern European latitudes molestus and pipiens populations occupy different habitats (underground vs. aboveground), a separation that most likely promotes genetic isolation between forms. However, the same does not hold in southern Europe where both forms occur aboveground in sympatry. In these southern habitats, the extent of hybridisation and its impact on the extent of genetic divergence between forms under sympatric conditions has not been clarified. For this purpose, we have used phenotypic and genetic data to characterise Cx. pipiens collected aboveground in Portugal. Our aims were to determine levels of genetic differentiation and the degree of hybridisation between forms occurring in sympatry, and to relate these with both evolutionary and epidemiological tenets of this biological group. Results: Autogeny and stenogamy was evaluated in the F1 progeny of 145 individual Cx. pipiens females. Bayesian clustering analysis based on the genotypes of 13 microsatellites revealed two distinct genetic clusters that were highly correlated with the alternative traits that define pipiens and molestus. Admixture analysis yielded hybrid rate estimates of 8-10%. Higher proportions of admixture were observed in pipiens individuals suggesting that more molestus genes are being introgressed into the pipiens form than the opposite. Conclusion: Both physiological/behavioural and genetic data provide evidence for the sympatric occurrence of molestus and pipiens forms of Cx. pipiens in the study area. In spite of the significant genetic differentiation between forms, hybridisation occurs at considerable levels. The observed pattern of asymmetric introgression probably relates to the different mating strategies adopted by each form. Furthermore, the differential introgression of molestus genes into the pipiens form may induce a more opportunistic biting behaviour in the latter thus potentiating its capacity to act as a bridge-vector for the transmission of arboviral infections.

Plant chemical defence: a partner control mechanism stabilising plant - seed-eating pollinator mutualisms.

Sebastien Ibanez — 2009-11-03T00:00:00Z

Background: Mutualisms are inherently conflictual as one partner always benefits from reducing the costs imposed by the other. Despite the widespread recognition that mutualisms are essentially reciprocal exploitation, there are few documented examples of traits that limit the costs of mutualism. In plant/seed-eating pollinator interactions the only mechanisms reported so far are those specific to one particular system, such as the selective abortion of over-exploited fruits. Results: This study shows that plant chemical defence against developing larvae constitutes another partner sanction mechanism in nursery mutualisms. It documents the chemical defence used by globeflower Trollius europaeus L. (Ranunculaceae) against the seed-eating larvae of six pollinating species of the genus Chiastocheta Pokorny (Anthomyiidae). The correlative field study carried out shows that the severity of damage caused by Chiastocheta larvae to globeflower fruits is linked to the accumulation in the carpel walls of a C-glycosyl-flavone (adonivernith), which reduces the larval seed predation ability per damaged carpel. The different Chiastocheta species do not exploit the fruit in the same way and their interaction with the plant chemical defence is variable, both in terms of induction intensity and larval sensitivity to adonivernith. Conclusion: Adonivernith accumulation and larval predation intensity appear to be both the reciprocal cause and effect. Adonivernith not only constitutes an effective chemical means of partner control, but may also play a key role in the sympatric diversification of the Chiastocheta genus.

Phylogenetic analysis of mitochondrial substitution rate variation in the angiosperm tribe Sileneae

Daniel Sloan — 2009-10-31T00:00:00Z

Background: Recent phylogenetic studies have revealed that the mitochondrial genome of the angiosperm Silene noctiflora (Caryophyllaceae) has experienced a massive mutation-driven acceleration in substitution rate, placing it among the fastest evolving eukaryotic genomes ever identified. To date, it appears that other species within Silene have maintained more typical substitution rates, suggesting that the acceleration in S. noctiflora is a recent and isolated evolutionary event. This assessment, however, is based on a very limited sampling of taxa within this diverse genus. Results: We analyzed the substitution rates in 4 mitochondrial genes (atp1, atp9, cox3 and nad9) across a broad sample of 74 species within Silene and related genera in the tribe Sileneae. We found that S. noctiflora shares its history of elevated mitochondrial substitution rate with the closely related species S. turkestanica. Another section of the genus (Conoimorpha) has experienced an acceleration of comparable magnitude. The phylogenetic data remain ambiguous as to whether the accelerations in these two clades represent independent evolutionary events or a single ancestral change. Rate variation among genes was equally dramatic. Most of the genus exhibited elevated rates for atp9 such that the average tree-wide substitution rate for this gene approached the values for the fastest evolving branches in the other three genes. In addition, some species exhibited major accelerations in atp1 and/or cox3 with no correlated change in other genes. Rates of non-synonymous substitution did not increase proportionally with synonymous rates but instead remained low and relatively invariant. Conclusion: The patterns of phylogenetic divergence within Sileneae suggest enormous variability in plant mitochondrial mutation rates and reveal a complex interaction of gene and species effects. The variation in rates across genomic and phylogenetic scales raises questions about the mechanisms responsible for the evolution of mutation rates in plant mitochondrial genomes.

Estimating the phylogeny and divergence times of primates using a supermatrix approach.

Helen Chatterjee — 2009-10-27T00:00:00Z

Background: The primates are among the most broadly studied mammalian orders, with the published literature containing extensive analyses of their behavior, physiology, genetics and ecology. The importance of this group in medical and biological research is well appreciated, and explains the numerous molecular phylogenies that have been proposed for most primate families and genera. Composite estimates for the entire order have been infrequently attempted, with the last phylogenetic reconstruction spanning the full range of primate evolutionary relationships having been conducted over a decade ago. Results: To estimate the structure and tempo of primate evolutionary history, we employed Bayesian phylogenetic methods to analyze data supermatrices comprising 7 mitochondrial genes (6,138 nucleotides) from 219 species across 67 genera and 3 nuclear genes (2,157 nucleotides) from 26 genera. Many taxa were only partially represented, with an average of 3.95 and 5.43 mitochondrial genes per species and per genus, respectively, and 2.23 nuclear genes per genus. Our analyses of mitochondrial DNA place Tarsiiformes as the sister group of Strepsirrhini. Within Haplorrhini, we find support for the primary divergence of Pitheciidae in Platyrrhini, and our results suggest a sister grouping of African and non-African colobines within Colobinae and of Cercopithecini and Papionini within Cercopthecinae. Date estimates for nodes within each family and genus are presented, with estimates for key splits including: Strepsirrhini-Haplorrhini 64 million years ago (MYA), Lemuriformes-Lorisiformes 52 MYA, Platyrrhini-Catarrhini 43 MYA and Cercopithecoidea-Hominoidea 29 MYA. Conclusion: We present an up-to-date, comprehensive estimate of the structure and tempo of primate evolutionary history. Although considerable gaps remain in our knowledge of the primate phylogeny, increased data sampling, particularly from nuclear loci, will be able to provide further resolution.