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Molecular biology and evolution [journal]
- Evolution of the cation chloride cotransporter family: ancient origins, gene-losses, and subfunctionalization through duplication. [JOURNAL ARTICLE]
- Mol Biol Evol 2013 Nov 21.
The cation chloride cotransporter (CCCs) family comprises of four subfamilies - K(+)-Cl(-) cotransporters (KCCs), Na(+)-K(+)-2Cl(-) cotransporters (NKCCs), Na(+)-Cl(-) cotransporters (NCCs) - and possibly two additional members - cation chloride cotransporter interacting protein (CIP1) and polyamine transporters (CCC9) - as well. Altogether, CCCs can play essential physiological roles in transepithelial ion reabsorption and secretion, cell volume regulation and inhibitory neurotransmission and so are present across all domains of life. To gain insight into the evolution of this family, we performed a comprehensive phylogenetic analysis using publically available genomic information. Our results clearly support CIP1 as being a true CCC based on shared evolutionary history. By contrast, the status of CCC9 in this regard remains equivocal. We also reveal the existence of a single ancestral CCC gene present in Archaea, from which numerous duplication events at the base of archaeans and eukaryotes lead to the divergence and subsequent neofunctionalization of the paralogous CCC subfamilies. A diversity of ensuing gene-loss events resulted in the complex distribution of CCCs present across the different taxa. Importantly, the occurrence of KCCs in "basal" metazoan taxa like sponges, would allow an early formation of fast hyperpolarizing neurotransmission in metazoans. Gene duplications within the CCC subfamilies in vertebrates (KCCs, NKCCs and NCCs in particular) lend further evidence to the 2R hypothesis of two rounds of genome duplication at the base of the vertebrate lineage, especially in concert with our syntenic cluster analyses. This increased number of KCCs, NKCCs and NCCs isoforms facilitates their further, important subfunctionalization in the vertebrate lineage.
- Selection-driven evolution of sex-biased genes is consistent with sexual selection in Arabidopsis thaliana. [JOURNAL ARTICLE]
- Mol Biol Evol 2013 Nov 21.
Sex-biased genes are genes with a preferential or specific expression in one sex and tend to show an accelerated rate of evolution in animals. Various hypotheses - which are not mutually exclusive - have been put forth to explain observed patterns of rapid evolution. One possible explanation is positive selection, but this has been shown only in few animal species and mostly for male-specific genes. Here we present a large-scale study that investigates evolutionary patterns of sex-biased genes in the predominantly self-fertilizing plant Arabidopsis thaliana. Unlike most animal species, A. thaliana does not possess sex chromosomes, its flowers develop both male and female sexual organs and it is characterized by low outcrossing rates. Using cell-specific gene expression data, we identified genes whose expression is enriched in comparison to all other tissues in the male and female gametes (sperm, egg, and central cell), as well as in synergids, pollen and pollen tubes, which also play an important role in reproduction. Genes specifically expressed in gametes and synergids show higher rates of protein evolution compared to the genome wide average and no evidence for positive selection. In contrast, pollen and pollen tube-specific genes have lower rates of protein evolution, but also exhibit a higher proportion of adaptive amino acid substitutions. We show that this is the result of increased levels of purifying and positive selection among genes with pollen and pollen tube-specific expression. The increased proportion of adaptive substitutions cannot be explained by the fact that pollen and pollen tube-expressed genes are enriched in segmental duplications, are on average older, or have a larger effective population size. Our observations are consistent with prezygotic sexual selection as a result of interactions during pollination and pollen tube growth such as pollen tube competition.
- A pluralistic account of homology: adapting the models to the data. [JOURNAL ARTICLE]
- Mol Biol Evol 2013 Nov 22.
Defining homologous genes is important in many evolutionary studies but raises obvious issues. Some of these issues are conceptual, and stem from our assumptions of how a gene evolves, others are practical, and depend on the algorithmic decisions implemented in existing software. Therefore, in order to make progress in the study of homology, both ontological and epistemological questions must be considered. In particular, defining homologous genes cannot solely be addressed under the classic assumptions of strong tree-thinking, according to which genes evolve in a strictly tree-like fashion of vertical descent and divergence and the problems of homology detection are primarily methodological. Gene homology could also be considered under a different perspective where genes evolve as 'public goods', subjected to various introgressive processes. In this latter case, defining homologous genes becomes a matter of designing models suited to the actual complexity of the data and how such complexity arises, rather than trying to fit genetic data to some a priori tree-like evolutionary model, a practice that inevitably results in the loss of much information. Here we show how important aspects of the problems raised by homology detection methods can be overcome when even more fundamental roots of these problems are addressed by analysing 'public goods thinking' evolutionary processes through which genes have frequently originated. This kind of thinking acknowledges distinct types of homologs, characterised by distinct patterns, in phylogenetic and non phylogenetic unrooted or multi-rooted networks. In addition, we define "family resemblances" to include genes that are related through intermediate relatives, thereby placing notions of homology in the broader context of evolutionary relationships. We conclude by presenting some pay-offs of adopting such a pluralistic account of homology and family relationship, that expands the scope of evolutionary analyses beyond the traditional, yet relatively narrow focus allowed by a strong tree-thinking view on gene evolution.
- Editor's Message for 2014. [JOURNAL ARTICLE]
- Mol Biol Evol 2013 Nov 22.
- FGF Signaling Emerged Concomitantly with the Origin of Eumetazoans. [JOURNAL ARTICLE]
- Mol Biol Evol 2013 Nov 30.
Complex metazoan bodies require cell-to-cell communication for development, a process often mediated by signaling molecules binding to specific receptors. Relatively few signaling pathways have been recruited during evolution to build multicellular animals from unicellular zygotes. Of these few signaling pathways, one of particular importance is the receptor tyrosine kinase (RTK) pathway. In metazoans, fibroblast growth factors (FGFs) bind to receptors in the RTK family, but the origin of the FGF gene family has so far remained a mystery. Here we show that extant bona fide FGFs most likely originated from proteins bearing an FGF-like domain that arose in a choanoflagellate/metazoan ancestor. We found orthologous genes closely related to FGF in choanoflagellates as well as in many metazoans such as sponges, acoels, protostomes, or nonvertebrate deuterostomes. We also show that these genes have a common evolutionary history with Retinitis Pigmentosa 1 (RP1). Even if some metazoan signaling pathways emerged long before multicellularity, we show that FGFs, like their receptors, originated in a eumetazoan ancestor.
- Differential Expression of Conserved Germ Line Markers and Delayed Segregation of Male and Female Primordial Germ Cells in a Hermaphrodite, the Leech Helobdella. [JOURNAL ARTICLE]
- Mol Biol Evol 2013 Nov 11.
In sexually reproducing animals, primordial germ cells (PGCs) are often set aside early in embryogenesis, a strategy that minimizes the risk of genomic damage associated with replication and mitosis during the cell cycle. Here, we have used germ line markers (piwi, vasa, and nanos) and microinjected cell lineage tracers to show that PGC specification in the leech genus Helobdella follows a different scenario: in this hermaphrodite, the male and female PGCs segregate from somatic lineages only after more than 20 rounds of zygotic mitosis; the male and female PGCs share the same (mesodermal) cell lineage for 19 rounds of zygotic mitosis. Moreover, while all three markers are expressed in both male and female reproductive tissues of the adult, they are expressed differentially between the male and female PGCs of the developing embryo: piwi and vasa are expressed preferentially in female PGCs at a time when nanos is expressed preferentially in male PGCs. A priori, the delayed segregation of male and female PGCs from somatic tissues and from one another increases the probability of mutations affecting both male and female PGCs of a given individual. We speculate that this suite of features, combined with a capacity for self-fertilization, may contribute to the dramatically rearranged genome of Helobdella robusta relative to other animals.
- A Guide for the Design of Evolve and Resequencing Studies. [JOURNAL ARTICLE]
- Mol Biol Evol 2013 Nov 28.
Standing genetic variation provides a rich reservoir of potentially useful mutations facilitating the adaptation to novel environments. Experimental evolution studies have demonstrated that rapid and strong phenotypic responses to selection can also be obtained in the laboratory. When combined with the next-generation sequencing technology, these experiments promise to identify the individual loci contributing to adaption. Nevertheless, until now, very little is known about the design of such evolve & resequencing (E&R) studies. Here, we use forward simulations of entire genomes to evaluate different experimental designs that aim to maximize the power to detect selected variants. We show that low linkage disequilibrium in the starting population, population size, duration of the experiment, and the number of replicates are the key factors in determining the power and accuracy of E&R studies. Furthermore, replication of E&R is more important for detecting the targets of selection than increasing the population size. Using an optimized design, beneficial loci with a selective advantage as low as s = 0.005 can be identified at the nucleotide level. Even when a large number of loci are selected simultaneously, up to 56% can be reliably detected without incurring large numbers of false positives. Our computer simulations suggest that, with an adequate experimental design, E&R studies are a powerful tool to identify adaptive mutations from standing genetic variation and thereby provide an excellent means to analyze the trajectories of selected alleles in evolving populations.
- Population Genomic Analysis Reveals No Evidence for GC-Biased Gene Conversion in Drosophila melanogaster. [JOURNAL ARTICLE]
- Mol Biol Evol 2013 Nov 28.
Gene conversion is the nonreciprocal exchange of genetic material between homologous chromosomes. Multiple lines of evidence from a variety of taxa strongly suggest that gene conversion events are biased toward GC-bearing alleles. However, in Drosophila, the data have largely been indirect and unclear, with some studies supporting the predictions of a GC-biased gene conversion model and other data showing contradictory findings. Here, we test whether gene conversion events are GC-biased in Drosophila melanogaster using whole-genome polymorphism and divergence data. Our results provide no support for GC-biased gene conversion and thus suggest that this process is unlikely to significantly contribute to patterns of polymorphism and divergence in this system.
- Comparative Dynamics and Distribution of Influenza Drug Resistance Acquisition to Protein M2 and Neuraminidase Inhibitors. [JOURNAL ARTICLE]
- Mol Biol Evol 2013 Nov 7.
Although efficient influenza vaccines are designed on a regular basis, the only protection of human populations against an unforeseen virus such as during the H1N1 pandemic in 2009 might be antiviral drugs. Adamantanes and neuraminidase inhibitors (Oseltamivir) represent two classes of such drugs that target the viral matrix protein 2 and neuraminidase, respectively. Although the emergence of resistance to both drugs has been described, the timing and spread of the acquisition of either single or dual resistances by different hosts is still unclear. Using a multilayered phylogenetic approach based on relaxed molecular clocks and large-scale maximum likelihood approaches, we show that Adamantane resistance evolved multiple times in various subtypes and hosts, possibly in breeding contexts (swine); and Oseltamivir resistance was also found in different subtypes and hosts, but its transmission is only sustained in humans. Furthermore, the dynamics of the emergence of antiviral resistance were examined for each drug. This showed that although the first mutations conferring resistance to Adamantanes precede US Food and Drug Administration (FDA) approval, general resistance emerged 15-38 years post-drug approval. This is in contrast to Oseltamivir resistance mutations that emerged at most 7 years after FDA approval of the drug. This study demonstrates the power of large-scale analyses to uncover and monitor the emergence dynamics of drug resistance.
- Society for molecular biology and evolution, council and business meetings, 2013, chicago, IL. [Journal Article]
- Mol Biol Evol 2013 Dec; 30(12):2733-4.