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      Is Open Access

      Composition and genomic organization of arthropod Hox clusters

      research-article
      , ,
      EvoDevo
      BioMed Central
      Hox, Evolution, Development, Arthropod, Chelicerate, Tetranychus, Ixodes, Daphnia, Segmentation

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          Abstract

          Background

          The ancestral arthropod is believed to have had a clustered arrangement of ten Hox genes. Within arthropods, Hox gene mutations result in transformation of segment identities. Despite the fact that variation in segment number/character was common in the diversification of arthropods, few examples of Hox gene gains/losses have been correlated with morphological evolution. Furthermore, a full appreciation of the variation in the genomic arrangement of Hox genes in extant arthropods has not been recognized, as genome sequences from each major arthropod clade have not been reported until recently. Initial genomic analysis of the chelicerate Tetranychus urticae suggested that loss of Hox genes and Hox gene clustering might be more common than previously assumed. To further characterize the genomic evolution of arthropod Hox genes, we compared the genomic arrangement and general characteristics of Hox genes from representative taxa from each arthropod subphylum.

          Results

          In agreement with others, we find arthropods generally contain ten Hox genes arranged in a common orientation in the genome, with an increasing number of sampled species missing either Hox3 or abdominal- A orthologs. The genomic clustering of Hox genes in species we surveyed varies significantly, ranging from 0.3 to 13.6 Mb. In all species sampled, arthropod Hox genes are dispersed in the genome relative to the vertebrate Mus musculus. Differences in Hox cluster size arise from variation in the number of intervening genes, intergenic spacing, and the size of introns and UTRs. In the arthropods surveyed, Hox gene duplications are rare and four microRNAs are, in general, conserved in similar genomic positions relative to the Hox genes.

          Conclusions

          The tightly clustered Hox complexes found in the vertebrates are not evident within arthropods, and differential patterns of Hox gene dispersion are found throughout the arthropods. The comparative genomic data continue to support an ancestral arthropod Hox cluster of ten genes with a shared orientation, with four Hox gene-associated miRNAs, although the degree of dispersion between genes in an ancestral cluster remains uncertain. Hox3 and abdominal- A orthologs have been lost in multiple, independent lineages, and current data support a model in which inversions of the Abdominal- B locus that result in the loss of abdominal- A correlate with reduced trunk segmentation.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s13227-016-0048-4) contains supplementary material, which is available to authorized users.

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          Most cited references81

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          A gene complex controlling segmentation in Drosophila.

          E B Lewis (1978)
          The bithorax gene complex in Drosophila contains a minimum of eight genes that seem to code for substances controlling levels of thoracic and abdominal development. The state of repression of at least four of these genes is controlled by cis-regulatory elements and a separate locus (Polycomb) seems to code for a repressor of the complex. The wild-type and mutant segmentation patterns are consistent with an antero-posterior gradient in repressor concentration along the embryo and a proximo-distal gradient along the chromosome in the affinities for repressor of each gene's cis-regulatory element.
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            The genome sequence of the malaria mosquito Anopheles gambiae.

            Anopheles gambiae is the principal vector of malaria, a disease that afflicts more than 500 million people and causes more than 1 million deaths each year. Tenfold shotgun sequence coverage was obtained from the PEST strain of A. gambiae and assembled into scaffolds that span 278 million base pairs. A total of 91% of the genome was organized in 303 scaffolds; the largest scaffold was 23.1 million base pairs. There was substantial genetic variation within this strain, and the apparent existence of two haplotypes of approximately equal frequency ("dual haplotypes") in a substantial fraction of the genome likely reflects the outbred nature of the PEST strain. The sequence produced a conservative inference of more than 400,000 single-nucleotide polymorphisms that showed a markedly bimodal density distribution. Analysis of the genome sequence revealed strong evidence for about 14,000 protein-encoding transcripts. Prominent expansions in specific families of proteins likely involved in cell adhesion and immunity were noted. An expressed sequence tag analysis of genes regulated by blood feeding provided insights into the physiological adaptations of a hematophagous insect.
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              The probability of duplicate gene preservation by subfunctionalization.

              It has often been argued that gene-duplication events are most commonly followed by a mutational event that silences one member of the pair, while on rare occasions both members of the pair are preserved as one acquires a mutation with a beneficial function and the other retains the original function. However, empirical evidence from genome duplication events suggests that gene duplicates are preserved in genomes far more commonly and for periods far in excess of the expectations under this model, and whereas some gene duplicates clearly evolve new functions, there is little evidence that this is the most common mechanism of duplicate-gene preservation. An alternative hypothesis is that gene duplicates are frequently preserved by subfunctionalization, whereby both members of a pair experience degenerative mutations that reduce their joint levels and patterns of activity to that of the single ancestral gene. We consider the ways in which the probability of duplicate-gene preservation by such complementary mutations is modified by aspects of gene structure, degree of linkage, mutation rates and effects, and population size. Even if most mutations cause complete loss-of-subfunction, the probability of duplicate-gene preservation can be appreciable if the long-term effective population size is on the order of 10(5) or smaller, especially if there are more than two independently mutable subfunctions per locus. Even a moderate incidence of partial loss-of-function mutations greatly elevates the probability of preservation. The model proposed herein leads to quantitative predictions that are consistent with observations on the frequency of long-term duplicate gene preservation and with observations that indicate that a common fate of the members of duplicate-gene pairs is the partitioning of tissue-specific patterns of expression of the ancestral gene.
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                Author and article information

                Contributors
                rmpace@bcm.edu
                mgrbic@uwo.ca
                520-626-2368 , lnagy@email.arizona.edu
                Journal
                EvoDevo
                Evodevo
                EvoDevo
                BioMed Central (London )
                2041-9139
                10 May 2016
                10 May 2016
                2016
                : 7
                : 11
                Affiliations
                [ ]Department of Molecular and Cellular Biology, University of Arizona, Tucson, AZ 85721 USA
                [ ]Department of Biology, University of Western Ontario, London, ON N6A 5B7 Canada
                [ ]Universidad de la Rioja, 26006 Logroño, Spain
                [ ]Division of Maternal-Fetal Medicine, Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, TX 77030 USA
                Author information
                http://orcid.org/0000-0002-8771-2603
                Article
                48
                10.1186/s13227-016-0048-4
                4862073
                27168931
                f3f779c2-3dd1-4211-8d0d-fcd9e04bd138
                © Pace et al. 2016

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 21 February 2016
                : 20 April 2016
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: DGE-0114420
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: T32GM008659
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000092, Ontario Genomics Institute;
                Award ID: OGI-046
                Award Recipient :
                Funded by: Ontario Research Fund–Global Leadership in Genomics and Life Sciences
                Award ID: GL2-01-035
                Award Recipient :
                Funded by: NSERC Strategic Grant
                Award ID: STPGP322206-05
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000076, Directorate for Biological Sciences;
                Award ID: NSF IOS 1024446
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2016

                Developmental biology
                hox,evolution,development,arthropod,chelicerate,tetranychus,ixodes,daphnia,segmentation
                Developmental biology
                hox, evolution, development, arthropod, chelicerate, tetranychus, ixodes, daphnia, segmentation

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