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BMC Evolutionary Biology - Latest articles
  • Parallel shifts in ecology and natural selection in an island lizard
    Background: Natural selection is a potent evolutionary force that shapes phenotypic variation to match ecological conditions. However, we know little about the year-to-year consistency of selection, or how inter-annual variation in ecology shapes adaptive landscapes and ultimately adaptive radiations. Methods: Here we combine remote sensing data, field experiments, and a four-year study of natural selection to show that changes in vegetation structure associated with a severe drought altered both habitat use and natural selection in the brown anole, Anolis sagrei. Results: In natural populations, lizards increased their use of vegetation in wet years and this was correlated with selection on limb length but not body size. By contrast, a die-back of vegetation caused by drought was followed by reduced arboreality, selection on body size, and relaxed selection on limb length. With the return of the rains and recovery of vegetation, selection reverted back to pre-drought pattern of selection acting on limb length but not body size. To test for the impact of vegetation loss on natural selection during the drought, we experimentally removed vegetation on a separate study island in a naturally wet year. The experiment revealed similar inter-annual changes in selection on body size but not limb length. Conclusion: Our results illustrate the dynamic nature of ecology driving natural selection on Anolis morphology and emphasize the importance of inter-annual environmental variation in shaping adaptive variation. In addition, results illustrate the utility of using remote sensing data to examine ecology's role in driving natural selection.

  • Evolution and differential expression of a vertebrate vitellogenin gene cluster
    Background: The multiplicity or loss of the vitellogenin (vtg) gene family in vertebrates has been argued to have broad implications for the mode of reproduction (placental or non-placental), cleavage pattern (meroblastic or holoblastic) and character of the egg (pelagic or benthic). Earlier proposals for the existence of three forms of vertebrate vtgs present conflicting models for their origin and subsequent duplication. Results: By integrating phylogenetics of novel vtg transcripts from old and modern teleosts with syntenic analyses of all available genomic variants of non-metatherian vertebrates we identify the gene orthologies between the Sarcopterygii (tetrapod branch) and Actinopterygii (fish branch). We argue that the vertebrate vtg gene cluster originated in proto-chromosome m, but that vtg genes have subsequently duplicated and rearranged following whole genome duplications. Sequencing of a novel fourth vtg transcript in labrid species, and the presence of duplicated paralogs in certain model organisms supports the notion that lineage-specific gene duplications frequently occur in teleosts. The data show that the vtg gene cluster is more conserved between acanthomorph teleosts and tetrapods, than in ostariophysan teleosts such as the zebrafish. The differential expression of the labrid vtg genes are further consistent with the notion that neofunctionalized Aa-type vtgs are important determinants of the pelagic or benthic character of the eggs in acanthomorph teleosts. Conclusion: The vertebrate vtg gene cluster existed prior to the separation of Sarcopterygii from Actinopterygii >450 million years ago, a period associated with the second round of whole genome duplication. The presence of higher copy numbers in a more highly expressed subcluster is particularly prevalent in teleosts. The differential expression and latent neofunctionalization of vtg genes in acanthomorph teleosts is an adaptive feature associated with oocyte hydration and spawning in the marine environment.

  • Phylogenetic relationships in Cortinarius, section Calochroi, inferred from nuclear DNA sequences
    Background: Section Calochroi is one of the most species-rich lineages in the genus Cortinarius (Agaricales, Basidiomycota) and is widely distributed across boreo-nemoral areas, with some extensions into meridional zones. Previous phylogenetic studies of Calochroi (incl. section Fulvi) have been geographically restricted; therefore, phylogenetic and biogeographic relationships within this lineage at a global scale have been largely unknown. In this study, we obtained DNA sequences from a broad taxon sampling from Europe, Central America and North America. We inferred intra- and interspecific phylogenetic relationships as well as major morphological evolutionary trends within section Calochroi based on 576 ITS sequences, 230 ITS + 5.8S + D1/D2 sequences, and a combined dataset of ITS + 5.8S + D1/D2 and RPB1 sequences of a representative subsampling of 58 species. Results: More than 100 species were identified by integrating DNA sequences with morphological, macrochemical and ecological data. We show that the section Calochroi is consistently resolved with relatively high nodal support into at least seven major lineages: Calochroi, Caroviolacei, Dibaphi, Elegantiores, Napi, Pseudoglaucopodes and Splendentes; whereas Rufoolivacei and Sulfurini appeared polyphyletic. A close relationship between Dibaphi, Elegantiores, Napi and Splendentes was consistently supported. Combinations of specific morphological, pigmentation and molecular characters appear useful in circumscribing clades. Conclusions: Our analyses demonstrate that Calochroi is an exclusively northern hemispheric lineage, where species follow their host trees throughout their natural ranges within and across continents. Results of this study have contributed substantially to defining European species in this group and will help to either identify or to name new species occurring across the northern hemisphere. Major groupings are in partial agreement with earlier morphology-based and molecular phylogenetic hypotheses, but some relationships were unexpected, based on external morphology. In such cases, their true affinities appear to have been obscured by the repeated appearance of similar features among distantly related species. Therefore, further taxonomic studies are needed to evaluate the consistency of species concepts and interpretations of morphological features in a more global context. Ancestral analyses indicate that there are two major evolutionary trends within section Calochroi: (1) the development of bright pigments evolved independently multiple times and (2) the evolution of abruptly marginate to flattened stipe bulbs represents an autapomorphy of the Calochroi clade.

  • EST based phylogenomics of Syndermata questions monophyly of Eurotatoria
    Background: The metazoan taxon Syndermata comprising Rotifera (in the classical sense of Monogononta+Bdelloidea+Seisonidea) and Acanthocephala has raised several theories connected to the phylogeny of these animal groups and the included subtaxa. While the monophyletic origin of Syndermata as well as of Acanthocephala is well established based on morphological and molecular data, the questions for a monophyletic origin of Monogononta, Bdelloidea, and Seisonidea and for the acanthocephalan sister group remain to be solved. Comparing the alternative hypotheses reveals that testing the phylogenetic validity of Eurotatoria (Monogononta+Bdelloidea) is the key to unravel the phylogenetic relations within Syndermata as a prerequisite for reconstructing the evolution of the acanthocephalan endoparasitism. Results: Here we present our results from a phylogenomic approach testing i) the monophyletic origin of monogononts and bdelloids and ii) their phylogenetic relations to acanthocephalans. For this analysis we have generated EST libraries of Pomphorhynchus laevis, Echinorhynchus truttae (both Palaeacanthocephala) and Brachionus plicatilis (Monogononta). By extending these data with database entries of Brachionus plicatilis (Monogononta), Philodina roseola (Bdelloidea) and 25 additional metazoan species, we conducted phylogenetic reconstructions based on 79 ribosomal proteins using maximum likelihood and bayesian approaches. Our findings strongly suggest that Eurotatoria are not monophyletic and that bdelloids are closer related to acanthocephalans than are monogononts. Conclusions: Mapping the morphological character evolution onto the molecular phylogeny suggests the emergence of a retractable anterior end (rostrum, proboscis) before the separation of Acanthocephala. This might have represented a key event leading to the later evolution of the acanthocephalan endoparasitism, given the enormous relevance of the proboscis for the anchoring of adult acanthocephalans to the definitive hosts' intestinal wall. If one further combines the present findings with previous support for Pararotatoria (Seisonidea+Acanthocephala) the rotatory organ might have undergone reduction before the separation of Acanthocephala, too.

  • Reconsidering the generation time hypothesis based on nuclear ribosomal ITS sequence comparisons in annual and perennial angiosperms.
    Background: Differences in plant annual/perennial habit are hypothesized to cause a generation time effect on divergence rates. Previous studies that compared rates of divergence for internal transcribed spacer (ITS1 and ITS2) sequences of nuclear ribosomal DNA (nrDNA) in angiosperms have reached contradictory conclusions about whether differences in generation times (or other life history features) are associated with divergence rate heterogeneity. We compared annual/perennial ITS divergence rates using published sequence data, employing sampling criteria to control for possible artifacts that might obscure any actual rate variation caused by annual/perennial differences. Results: Relative rate tests employing ITS sequences from 16 phylogenetically-independent annual/perennial species pairs rejected rate homogeneity in only a few comparisons, with annuals more frequently exhibiting faster substitution rates. Treating branch length differences categorically (annual faster or perennial faster regardless of magnitude) with a sign test often indicated an excess of annuals with faster substitution rates. Annuals showed an approximately 1.6-fold rate acceleration in nucleotide substitution models for ITS. Relative rates of three nuclear loci and two chloroplast regions for the annual Arabidopsis thaliana compared with two closely related Arabidopsis perennials indicated that divergence was faster for the annual. In contrast, A. thaliana ITS divergence rates were sometimes faster and sometimes slower than the perennial. In simulations, divergence rate differences of at least 3.5-fold were required to reject rate constancy in >80 % of replicates using a nucleotide substitution model observed for the combination of ITS1 and ITS2. Simulations also showed that categorical treatment of branch length differences detected rate heterogeneity >80% of the time with a 1.5-fold or greater rate difference. Conclusions: Although rate homogeneity was not rejected in many comparisons, in cases of significant rate heterogeneity annuals frequently exhibited faster substitution rates. Our results suggest that annual taxa may exhibit a less than 2-fold rate acceleration at ITS. Since the rate difference is small and ITS lacks statistical power to reject rate homogeneity, further studies with greater power will be required to adequately test the hypothesis that annual and perennial plants have heterogeneous substitution rates. Arabidopsis sequence data suggest that relative rate tests based on multiple loci may be able to distinguish a weak acceleration in annual plants. The failure to detect rate heterogeneity with ITS in past studies may be largely a product of low statistical power.

  • Differential selection on gene translation efficiency between the filamentous fungus Ashbya gossypii and yeasts
    Background: The filamentous fungus Ashbya gossypii grows into a multicellular mycelium that is distinct from the unicellular morphology of its closely related yeast species. It has been proposed that genes important for cell cycle regulation play central roles for such phenotypic differences. Because A. gossypii shares an almost identical set of cell cycle genes with the typical yeast Saccharomyces cerevisiae, the differences might occur at the level of orthologous gene regulation. Codon usage patterns were compared to identify orthologous genes with different gene regulation between A. gossypii and nine closely related yeast species. Results: Here we identified 3,151 orthologous genes between A. gossypii and nine yeast species. Two groups of genes with significant differences in codon usage (gene translation efficiency) were identified between A. gossypii and yeasts. 333 genes (Group I) and 552 genes (Group II) have significantly higher translation efficiency in A. gossypii and yeasts, respectively. Functional enrichment and pathway analysis show that Group I genes are significantly enriched with cell cycle functions whereas Group II genes are biased toward metabolic functions. Conclusions: Because translation efficiency of a gene is closely related to its functional importance, the observed functional distributions of orthologous genes with different translation efficiency might account for phenotypic differentiation between A. gossypii and yeast species. The results shed light on the mechanisms for pseudohyphal growth in pathogenic yeast species.

  • Genetic characterization of the ABO blood group in Neandertals
    Background: The high polymorphism rate in the human ABO blood group gene seems to be related to susceptibility to different pathogens. It has been estimated that all genetic variation underlying the human ABO alleles appeared along the human lineage, after the divergence from the chimpanzee lineage. A paleogenetic analysis of the ABO blood group gene in Neandertals allows us to directly test for the presence of the ABO alleles in these extinct humans. Results: We have analysed two male Neandertals that were retrieved under controlled conditions at the El Sidron site in Asturias (Spain) and that appeared to be almost free of modern human DNA contamination. We find a human specific diagnostic deletion for blood group O (O01 haplotype) in both Neandertal individuals. Conclusions: These results suggest that the genetic change responsible for the O blood group in humans predates the human and Neandertal divergence. A potential selective event associated with the emergence of the O allele may have therefore occurred after humans separated from their common ancestor with chimpanzees and before the human-Neandertal population divergence.

  • Oceanic dispersal barriers, adaptation and larval retention: an interdisciplinary assessment of potential factors maintaining a phylogeographic break between sister lineages of an African prawn.
    Background: Genetic breaks separating regional lineages of marine organisms with potentially high broadcasting abilities are generally attributed either to dispersal barriers such as currents or upwelling, or to behavioural strategies promoting self-recruitment. We investigated whether such patterns could potentially also be explained by adaptations to different environmental conditions by studying two morphologically distinguishable genetic lineages of the estuarine mudprawn Upogebia africana across a biogeographic disjunction in south-eastern Africa. The study area encompasses a transition between temperate and subtropical biotas, where the warm, southward-flowing Agulhas Current is deflected away from the coast, and its inshore edge is characterised by intermittent upwelling. To determine how this phylogeographic break is maintained, we estimated gene flow among populations in the region, tested for isolation by distance as an indication of larval retention, and reared larvae of the temperate and subtropical lineages at a range of different temperatures. Results: Of four populations sampled, the two northernmost exclusively included the subtropical lineage, a central population had a mixture of both lineages, and the southernmost estuary had only haplotypes of the temperate lineage. No evidence was found for isolation by distance, and gene flow was bidirectional and of similar magnitude among adjacent populations. In both lineages, the optimum temperature for larval development was at about 23oC, but a clear difference was found at lower temperatures. While larvae of the temperate lineage could complete development at temperatures as low as 12oC, those of the subtropical lineage did not complete development below 17oC. Conclusions: The results indicate that both southward dispersal of the subtropical lineage inshore of the Agulhas Current, and its establishment in the temperate province, may be limited primarily by low water temperatures. There is no evidence that the larvae of the temperate lineage would survive less well in the subtropical province than in their native habitat, and their exclusion from this region may be due to a combination of upwelling, short larval duration with limited dispersal potential near the coast, plus transport away from the coast of larvae that become entrained in the Agulhas Current. This study shows how methods from different fields of research (genetics, physiology, oceanography and morphology) can be combined to study phylogeographic patterns.

  • Evolutionary history of the fish genus Astyanax Baird & Girard (1854) (Actynopterigii, Characidae) in Mesoamerica reveals multiple morphological homoplasies
    Background: Mesoamerica represents a complex biogeographical region in the world, mostly due to its geological history. This complexity has lead to interesting biogeographical patterns that have shaped the actual diversity and distribution of the fauna in the region. The fish genus Astyanax represents an accurate model to access to these patterns due to its high phenotypic plasticity and because is the most diverse and is the widest distributed freshwater fish in America. In our study we used mitochondrial and nuclear DNA data to establish the phylogenetic relationships within the genus in Mesoamerica and develop historical biogeographical hypothesis to explain its current distribution. Results: Two independent analyses (Cyt b, 1140 bp and including 208 individuals from 147 localities and a combined matrix with Cyt b, 16S, COI and RAG1, for a subset of data) yielded similar topologies, recovering six major groups with phylogeographic structure. North America and Upper Central America were monophyletic, while Middle Central America represented a rapid radiation where relationships were not fully resolved. Lower Central America lineages showed a fragmented structure, with a very restricted distribution and high molecular divergence. All Bramocharax samples were included in different Astyanax lineages, with less than 1% of divergence with sympatric or allopatric Astyanax, giving additional evidence of the homoplasic nature of trophic specializations, which have evolved during independent evolutionary episodes and in different places. We observed a higher taxonomic diversity compared to previous phylogenetic studies. Mesoamerica colonization Astyanax was previous to the final closure of the Isthmus of Panama (6-8 Mya), leading to a fragmented configuration of Lower Central America. Additionally in upper part of Mesoamerica we observed two independent colonization tracks showing a turnover lineage process. Conclusions: Our results support a multiple and independent origin of morphological traits in this genus, where the Bramocharax genus morphotype represents a recurrent trophic adaptations of Astyanax. The presence of Astyanax in Mesoamerica was during the Miocene (~8 Mya) suggesting an incipient land bridge connecting South America and Central America, previous to the final closure of the Panama Isthmus (~3.3 Mya).

  • Phylogeography and historical demography of the Lusitanian snail Elona quimperiana reveal survival in unexpected separate glacial refugia.
    Background: Present day distributions of Palearctic taxa in northern latitudes mainly result from populations having survived in local patches during the Late Pleistocene and/or from recolonizing populations from southern temperate refugia. If well-studied Mediterranean and eastern European refugia are widely accepted, some recent biogeographical assumptions still remain unclear, such as the occurrence of multiple glacial refugia in Iberia and cryptic refugia in northern Europe during the last glaciations. The Lusitanian snail Elona quimperiana has a remarkably disjunct distribution, limited to northwestern France (Brittany), northwestern Spain and the Basque Country. By describing the phylogeographical structure of this species across its entire range, the present study attempts to identify refugia and subsequent recolonization routes. Results: Results based on 16S and COI gene sequences showed that the low genetic diversity observed in the Brittany populations should be associated with a recent demographic expansion. By contrast, populations from Spain exhibit several differentiated lineages and are characterized by demographic equilibrium, while the Basque populations are the only ones harboring typical distinct haplotypes. The center of the star-like networks of both gene sequences is occupied by a common ancestral-like haplotype found in Brittany and Spain, which might have originated from the middle of Northern Spain (i.e. Asturias, eastern Lugo and western Cantabria). Estimates of the divergence time between the Spain-Brittany and Basque lineages strongly suggest that E. quimperiana survived the Pleistocene glaciations in distinct refugia on the Iberian Peninsula, one of which is situated in Picos de Europa, and the other in the Basque Country. The occurrence of a northern refugium in France cannot be rejected as of yet. Conclusions: Present results confirm the Iberian origin of the land snail E. quimperiana and strongly support the emerging phylogeographic hypothesis of multiple refugia in Iberia during the last glaciations. The scenario of a spatial expansion of E. quimperiana from an Iberian refuge located in Asturias to northern areas provides the most probable explanation for the present distribution of this land snail. By harboring distinct haplotypes, the Basque Country populations appear to be of great importance in terms of potential adaptation, long term persistence and hence, the conservation of E. quimperiana.


Robyne Wilkerson
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