Publications by authors named "Artyom Kopp"

63 Publications

Evolution of sexual development and sexual dimorphism in insects.

Curr Opin Genet Dev 2021 Apr 10;69:129-139. Epub 2021 Apr 10.

Department of Evolution and Ecology, University of California, One Shields Ave, Davis, CA, 95616, USA.

Most animal species consist of two distinct sexes. At the morphological, physiological, and behavioral levels the differences between males and females are numerous and dramatic, yet at the genomic level they are often slight or absent. This disconnect is overcome because simple genetic differences or environmental signals are able to direct the sex-specific expression of a shared genome. A canonical picture of how this process works in insects emerged from decades of work on Drosophila. But recent years have seen an explosion of molecular-genetic and developmental work on a broad range of insects. Drawing these studies together, we describe the evolution of sexual dimorphism from a comparative perspective and argue that insect sex determination and differentiation systems are composites of rapidly evolving and highly conserved elements.
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http://dx.doi.org/10.1016/j.gde.2021.02.011DOI Listing
April 2021

A phylogeny for the Drosophila montium species group: A model clade for comparative analyses.

Mol Phylogenet Evol 2021 May 31;158:107061. Epub 2020 Dec 31.

Department of Evolution and Ecology, University of California, Davis, CA 95616, USA. Electronic address:

The Drosophila montium species group is a clade of 94 named species, closely related to the model species D. melanogaster. The montium species group is distributed over a broad geographic range throughout Asia, Africa, and Australasia. Species of this group possess a wide range of morphologies, mating behaviors, and endosymbiont associations, making this clade useful for comparative analyses. We use genomic data from 42 available species to estimate the phylogeny and relative divergence times within the montium species group, and its relative divergence time from D. melanogaster. To assess the robustness of our phylogenetic inferences, we use 3 non-overlapping sets of 20 single-copy coding sequences and analyze all 60 genes with both Bayesian and maximum likelihood methods. Our analyses support monophyly of the group. Apart from the uncertain placement of a single species, D. baimaii, our analyses also support the monophyly of all seven subgroups proposed within the montium group. Our phylograms and relative chronograms provide a highly resolved species tree, with discordance restricted to estimates of relatively short branches deep in the tree. In contrast, age estimates for the montium crown group, relative to its divergence from D. melanogaster, depend critically on prior assumptions concerning variation in rates of molecular evolution across branches, and hence have not been reliably determined. We discuss methodological issues that limit phylogenetic resolution - even when complete genome sequences are available - as well as the utility of the current phylogeny for understanding the evolutionary and biogeographic history of this clade.
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http://dx.doi.org/10.1016/j.ympev.2020.107061DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7946709PMC
May 2021

A hierarchical Bayesian mixture model for inferring the expression state of genes in transcriptomes.

Proc Natl Acad Sci U S A 2020 08 24;117(32):19339-19346. Epub 2020 Jul 24.

Department of Evolution and Ecology, University of California, Davis, CA 95616.

Transcriptomes are key to understanding the relationship between genotype and phenotype. The ability to infer the expression state (active or inactive) of genes in the transcriptome offers unique benefits for addressing this issue. For example, qualitative changes in gene expression may underly the origin of novel phenotypes, and expression states are readily comparable between tissues and species. However, inferring the expression state of genes is a surprisingly difficult problem, owing to the complex biological and technical processes that give rise to observed transcriptomic datasets. Here, we develop a hierarchical Bayesian mixture model that describes this complex process and allows us to infer expression state of genes from replicate transcriptomic libraries. We explore the statistical behavior of this method with analyses of simulated datasets-where we demonstrate its ability to correctly infer true (known) expression states-and empirical-benchmark datasets, where we demonstrate that the expression states inferred from RNA-sequencing (RNA-seq) datasets using our method are consistent with those based on independent evidence. The power of our method to correctly infer expression states is generally high and remarkably, approaches the maximum possible power for this inference problem. We present an empirical analysis of primate-brain transcriptomes, which identifies genes that have a unique expression state in humans. Our method is implemented in the freely available R package zigzag.
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http://dx.doi.org/10.1073/pnas.1919748117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7431084PMC
August 2020

Evolution of sexually dimorphic pheromone profiles coincides with increased number of male-specific chemosensory organs in .

Ecol Evol 2019 Dec 17;9(23):13608-13618. Epub 2019 Nov 17.

Department of Evolution and Ecology University of California-Davis Davis CA USA.

Binary communication systems that involve sex-specific signaling and sex-specific signal perception play a key role in sexual selection and in the evolution of sexually dimorphic traits. The driving forces and genetic changes underlying such traits can be investigated in systems where sex-specific signaling and perception have emerged recently and show evidence of potential coevolution. A promising model is found in , which exhibits a species-specific increase in the number of male chemosensory bristles. We show that this transition coincides with recent evolutionary changes in cuticular hydrocarbon (CHC) profiles. Long-chain CHCs that are sexually monomorphic in the closest relatives of (, , , and ) are strongly male-biased in this species. We also identify an intraspecific female-limited polymorphism, where some females have male-like CHC profiles. Both the origin of sexually dimorphic CHC profiles and the female-limited polymorphism in involve changes in the relative amounts of three mono-alkene homologs, 9-tricosene, 9-pentacosene, and 9-heptacosene, all of which share a common biosynthetic origin and point to a potentially simple genetic change underlying these traits. Our results suggest that pheromone synthesis may have coevolved with chemosensory perception and open the way for reconstructing the origin of sexual dimorphism in this communication system.
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http://dx.doi.org/10.1002/ece3.5819DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6912897PMC
December 2019

Sex-specific evolution of relative leg size in Drosophila prolongata results from changes in the intersegmental coordination of tissue growth.

Evolution 2019 11 22;73(11):2281-2294. Epub 2019 Oct 22.

Department of Evolution and Ecology, University of California-Davis, Davis, California, 95616.

Evolution of relative organ size is the most prolific source of morphological diversity, yet the underlying molecular mechanisms that modify growth control are largely unknown. Models where organ proportions have undergone recent evolutionary changes hold the greatest promise for understanding this process. Uniquely among Drosophila species, Drosophila prolongata displays a dramatic, male-specific increase in the size of its forelegs relative to other legs. By comparing leg development between males and females of D. prolongata and its closest relative Drosophila carrolli, we show that the exaggerated male forelegs are produced by a sex- and segment-specific increase in mitosis during the final larval instar. Intersegmental compensatory control, where smaller leg primordia grow at a faster rate, is observed in both species and sexes. However, the equilibrium growth rates that determine the final relative proportion between the first and second legs have shifted in male D. prolongata compared both to conspecific females and to D. carrolli. We suggest that the observed developmental changes that produce new adult proportions reflect an interplay between conserved growth coordination mechanisms and evolving organ-specific growth targets.
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http://dx.doi.org/10.1111/evo.13847DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6834887PMC
November 2019

Hemimetabolous insects elucidate the origin of sexual development via alternative splicing.

Elife 2019 09 3;8. Epub 2019 Sep 3.

Department of Evolution and Ecology, University of California, Davis, Davis, United States.

Insects are the only known animals in which sexual differentiation is controlled by sex-specific splicing. The transcription factor produces distinct male and female isoforms, which are both essential for sex-specific development. splicing depends on , which is also alternatively spliced such that functional Tra is only present in females. This pathway has evolved from an ancestral mechanism where was independent of and expressed and required only in males. To reconstruct this transition, we examined three basal, hemimetabolous insect orders: Hemiptera, Phthiraptera, and Blattodea. We show that and have distinct functions in these insects, reflecting different stages in the changeover from a transcription-based to a splicing-based mode of sexual differentiation. We propose that the canonical insect pathway evolved via merger between expanding function (from males to both sexes) and narrowing function (from a general splicing factor to dedicated regulator of ).
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http://dx.doi.org/10.7554/eLife.47490DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6721801PMC
September 2019

Modular tissue-specific regulation of underpins sexually dimorphic development in .

Development 2019 07 25;146(14). Epub 2019 Jul 25.

Department of Evolution and Ecology, University of California-Davis, Davis, CA 95616, USA

The ability of a single genome to produce distinct and often dramatically different male and female forms is one of the wonders of animal development. In , most sexually dimorphic traits are controlled by sex-specific isoforms of the () transcription factor, and expression is mostly limited to cells that give rise to sexually dimorphic traits. However, it is unknown how this mosaic of sexually dimorphic and monomorphic organs arises. Here, we characterize the -regulatory sequences that control expression in the foreleg, which contains multiple types of sex-specific sensory organs. We find that separate modular enhancers are responsible for expression in each sexually dimorphic organ. Expression of in the sex comb is co-regulated by two enhancers with distinct spatial and temporal specificities that are separated by a genitalia-specific enhancer. The sex comb-specific enhancer from , a species that primitively lacks sex combs, is not active in the foreleg. Thus, the mosaic of sexually dimorphic and monomorphic organs depends on modular regulation of transcription by dedicated cell type-specific enhancers.
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http://dx.doi.org/10.1242/dev.178285DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6679366PMC
July 2019

Drosophila (Sophophora) carrolli n. sp., a new species from Brunei, closely related to Drosophila (Sophophora) rhopaloa Bock Wheeler, 1972 (Diptera: Drosophilidae).

Zootaxa 2018 Jun 18;4434(3):502-510. Epub 2018 Jun 18.

Ludwig-Maximilians Universität München, Fakultät für Biologie, Biozentrum, Großhaderner Strasse 2, 82152 Planegg-Martinsried, Germany..

We describe a new species in the Drosophila melanogaster species group, Drosophila carrolli n. sp., showing morphological affinities with D. rhopaloa Bock Wheeler, 1972.
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http://dx.doi.org/10.11646/zootaxa.4434.3.6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6438695PMC
June 2018

A Distalless-responsive enhancer of the Hox gene Sex combs reduced is required for segment- and sex-specific sensory organ development in Drosophila.

PLoS Genet 2018 04 10;14(4):e1007320. Epub 2018 Apr 10.

Department of Biological Sciences, University of Illinois at Chicago, Chicago, IL, United States of America.

Hox genes are involved in the patterning of animal body parts at multiple levels of regulatory hierarchies. Early expression of Hox genes in different domains along the embryonic anterior-posterior (A/P) axis in insects, vertebrates, and other animals establishes segmental or regional identity. However, Hox gene function is also required later in development for the patterning and morphogenesis of limbs and other organs. In Drosophila, spatiotemporal modulation of Sex combs reduced (Scr) expression within the first thoracic (T1) leg underlies the generation of segment- and sex-specific sense organ patterns. High Scr expression in defined domains of the T1 leg is required for the development of T1-specific transverse bristle rows in both sexes and sex combs in males, implying that the patterning of segment-specific sense organs involves incorporation of Scr into the leg development and sex determination gene networks. We sought to gain insight into this process by identifying the cis-and trans-regulatory factors that direct Scr expression during leg development. We have identified two cis-regulatory elements that control spatially modulated Scr expression within T1 legs. One of these enhancers directs sexually dimorphic expression and is required for the formation of T1-specific bristle patterns. We show that the Distalless and Engrailed homeodomain transcription factors act through sequences in this enhancer to establish elevated Scr expression in spatially defined domains. This enhancer functions to integrate Scr into the intrasegmental gene regulatory network, such that Scr serves as a link between leg patterning, sex determination, and sensory organ development.
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http://dx.doi.org/10.1371/journal.pgen.1007320DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5909922PMC
April 2018

Evolving doublesex expression correlates with the origin and diversification of male sexual ornaments in the Drosophila immigrans species group.

Evol Dev 2018 03 25;20(2):78-88. Epub 2018 Jan 25.

Department of Evolution and Ecology, University of California-Davis, Davis, California.

Male ornaments and other sex-specific traits present some of the most dramatic examples of evolutionary innovations. Comparative studies of similar but independently evolved traits are particularly important for identifying repeated patterns in the evolution of these traits. Male-specific modifications of the front legs have evolved repeatedly in Drosophilidae and other Diptera. The best understood of these novel structures is the sex comb of Drosophila melanogaster and its close relatives. Here, we examine the evolution of another male foreleg modification, the sex brush, found in the distantly related Drosophila immigrans species group. Similar to the sex comb, we find that the origin of the sex brush correlates with novel, spatially restricted expression of the doublesex (dsx) transcription factor, the primary effector of the Drosophila sex determination pathway. The diversity of Dsx expression patterns in the immigrans species group closely reflects the differences in the presence, position, and size of the sex brush. Together with previous work on sex comb evolution, these observations suggest that tissue-specific activation of dsx expression may be a common mechanism responsible for the evolution of sexual dimorphism and particularly for the origin of novel male-specific ornaments.
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http://dx.doi.org/10.1111/ede.12249DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6444933PMC
March 2018

Single-Molecule Sequencing of the Genome.

G3 (Bethesda) 2017 03 10;7(3):781-788. Epub 2017 Mar 10.

School of Biological Sciences, The University of Queensland, St Lucia, Queensland 4072, Australia

Long-read sequencing technology promises to greatly enhance assembly of genomes for nonmodel species. Although the error rates of long reads have been a stumbling block, sequencing at high coverage permits the self-correction of many errors. Here, we sequence and assemble the genome of , a species from the subgroup that has been well-studied for latitudinal clines, sexual selection, and gene expression, but which lacks a reference genome. Using 11 PacBio single-molecule real-time (SMRT cells), we generated 12 Gbp of raw sequence data comprising ∼65 × whole-genome coverage. Read lengths averaged 8940 bp (NRead50 12,200) with the longest read at 53 kbp. We self-corrected reads using the PBDagCon algorithm and assembled the genome using the MHAP algorithm within the PBcR assembler. Total genome length was 198 Mbp with an N50 just under 1 Mbp. Contigs displayed a high degree of chromosome arm-level conservation with the genome and many could be sensibly placed on the physical map. We also provide an initial annotation for this genome using gene predictions that were supported by RNA-seq data.
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http://dx.doi.org/10.1534/g3.116.037598DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5345708PMC
March 2017

Genetic Convergence in the Evolution of Male-Specific Color Patterns in Drosophila.

Curr Biol 2016 09 18;26(18):2423-2433. Epub 2016 Aug 18.

Department of Evolution and Ecology, University of California, Davis, Davis, CA 95616, USA.

Convergent evolution provides a type of natural replication that can be exploited to understand the roles of contingency and constraint in the evolution of phenotypes and the gene networks that control their development. For sex-specific traits, convergence offers the additional opportunity for testing whether the same gene networks follow different evolutionary trends in males versus females. Here, we use an unbiased, systematic mapping approach to compare the genetic basis of evolutionary changes in male-limited pigmentation in several pairs of Drosophila species that represent independent evolutionary transitions. We find strong evidence for repeated recruitment of the same genes to specify similar pigmentation in different species. At one of these genes, ebony, we observe convergent evolution of sexually dimorphic and monomorphic expression through cis-regulatory changes. However, this functional convergence has a different molecular basis in different species, reflecting both parallel fixation of ancestral alleles and independent origin of distinct mutations with similar functional consequences. Our results show that a strong evolutionary constraint at the gene level is compatible with a dominant role of chance at the molecular level.
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http://dx.doi.org/10.1016/j.cub.2016.07.034DOI Listing
September 2016

The pdm3 Locus Is a Hotspot for Recurrent Evolution of Female-Limited Color Dimorphism in Drosophila.

Curr Biol 2016 09 18;26(18):2412-2422. Epub 2016 Aug 18.

Department of Evolution and Ecology, University of California, Davis, 1 Shields Avenue, Davis, CA 95616, USA. Electronic address:

Sex-limited polymorphisms are an intriguing form of sexual dimorphism that offer unique opportunities to reconstruct the evolutionary changes that decouple male and female traits encoded by a shared genome. We investigated the genetic basis of a Mendelian female-limited color dimorphism (FLCD) that segregates in natural populations of more than 20 species of the Drosophila montium subgroup. In these species, females have alternative abdominal color morphs, light and dark, whereas males have only one color morph in each species. A comprehensive molecular phylogeny of the montium subgroup supports multiple origins of FLCD. Despite this, we mapped FLCD to the same locus in four distantly related species-the transcription factor POU domain motif 3 (pdm3), which acts as a repressor of abdominal pigmentation in D. melanogaster. In D. serrata, FLCD maps to a structural variant in the first intron of pdm3; however, this variant is not found in the three other species-D. kikkawai, D. leontia, and D. burlai-and sequence analysis strongly suggests the pdm3 alleles responsible for FLCD originated independently at least three times. We propose that cis-regulatory changes in pdm3 form sexually dimorphic and monomorphic alleles that segregate within species and are preserved, at least in one species, by structural variation. Surprisingly, pdm3 has not been implicated in the evolution of sex-specific pigmentation outside the montium subgroup, suggesting that the genetic paths to sexual dimorphism may be constrained within a clade but variable across clades.
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http://dx.doi.org/10.1016/j.cub.2016.07.016DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5450831PMC
September 2016

Interactions between Drosophila and its natural yeast symbionts-Is Saccharomyces cerevisiae a good model for studying the fly-yeast relationship?

PeerJ 2015 25;3:e1116. Epub 2015 Aug 25.

Department of Evolution and Ecology and Center for Population Biology, University of California , Davis, CA , USA ; Current affiliation: Department of Molecular and Cellular Biology, University of California , Berkeley, CA , USA.

Yeasts play an important role in the biology of the fruit fly, Drosophila melanogaster. In addition to being a valuable source of nutrition, yeasts affect D. melanogaster behavior and interact with the host immune system. Most experiments investigating the role of yeasts in D. melanogaster biology use the baker's yeast, Saccharomyces cerevisiae. However, S. cerevisiae is rarely found with natural populations of D. melanogaster or other Drosophila species. Moreover, the strain of S. cerevisiae used most often in D. melanogaster experiments is a commercially and industrially important strain that, to the best of our knowledge, was not isolated from flies. Since disrupting natural host-microbe interactions can have profound effects on host biology, the results from D. melanogaster-S. cerevisiae laboratory experiments may not be fully representative of host-microbe interactions in nature. In this study, we explore the D. melanogaster-yeast relationship using five different strains of yeast that were isolated from wild Drosophila populations. Ingested live yeasts have variable persistence in the D. melanogaster gastrointestinal tract. For example, Hanseniaspora occidentalis persists relative to S. cerevisiae, while Brettanomyces naardenensis is removed. Despite these differences in persistence relative to S. cerevisiae, we find that all yeasts decrease in total abundance over time. Reactive oxygen species (ROS) are an important component of the D. melanogaster anti-microbial response and can inhibit S. cerevisiae growth in the intestine. To determine if sensitivity to ROS explains the differences in yeast persistence, we measured yeast growth in the presence and absence of hydrogen peroxide. We find that B. naardenesis is completely inhibited by hydrogen peroxide, while H. occidentalis is not, which is consistent with yeast sensitivity to ROS affecting persistence within the D. melanogaster gastrointestinal tract. We also compared the feeding preference of D. melanogaster when given the choice between a naturally associated yeast and S. cerevisiae. We do not find a correlation between preferred yeasts and those that persist in the intestine. Notably, in no instances is S. cerevisiae preferred over the naturally associated strains. Overall, our results show that D. melanogaster-yeast interactions are more complex than might be revealed in experiments that use only S. cerevisiae. We propose that future research utilize other yeasts, and especially those that are naturally associated with Drosophila, to more fully understand the role of yeasts in Drosophila biology. Since the genetic basis of host-microbe interactions is shared across taxa and since many of these genes are initially discovered in D. melanogaster, a more realistic fly-yeast model system will benefit our understanding of host-microbe interactions throughout the animal kingdom.
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http://dx.doi.org/10.7717/peerj.1116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4556146PMC
September 2015

Comparative validation of the D. melanogaster modENCODE transcriptome annotation.

Genome Res 2014 Jul;24(7):1209-23

Human Genome Sequencing Center, Baylor College of Medicine, Houston, Texas 77030, USA;

Accurate gene model annotation of reference genomes is critical for making them useful. The modENCODE project has improved the D. melanogaster genome annotation by using deep and diverse high-throughput data. Since transcriptional activity that has been evolutionarily conserved is likely to have an advantageous function, we have performed large-scale interspecific comparisons to increase confidence in predicted annotations. To support comparative genomics, we filled in divergence gaps in the Drosophila phylogeny by generating draft genomes for eight new species. For comparative transcriptome analysis, we generated mRNA expression profiles on 81 samples from multiple tissues and developmental stages of 15 Drosophila species, and we performed cap analysis of gene expression in D. melanogaster and D. pseudoobscura. We also describe conservation of four distinct core promoter structures composed of combinations of elements at three positions. Overall, each type of genomic feature shows a characteristic divergence rate relative to neutral models, highlighting the value of multispecies alignment in annotating a target genome that should prove useful in the annotation of other high priority genomes, especially human and other mammalian genomes that are rich in noncoding sequences. We report that the vast majority of elements in the annotation are evolutionarily conserved, indicating that the annotation will be an important springboard for functional genetic testing by the Drosophila community.
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http://dx.doi.org/10.1101/gr.159384.113DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4079975PMC
July 2014

The genetics of sex: exploring differences.

Genetics 2014 Jun;197(2):527-9

Biology Department, Johns Hopkins University, Baltimore, Maryland 21218.

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http://dx.doi.org/10.1534/genetics.114.165456DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4063912PMC
June 2014

The genetics of sex: exploring differences.

G3 (Bethesda) 2014 Jun 17;4(6):979-81. Epub 2014 Jun 17.

Biology Department, Johns Hopkins University, Baltimore, Maryland 21218.

In this commentary, Michelle Arbeitman et al., examine the topic of the Genetics of Sex as explored in this month's issues of GENETICS and G3: Genes|Genomes|Genetics. These inaugural articles are part of a joint Genetics of Sex collection (ongoing) in the GSA journals.
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http://dx.doi.org/10.1534/g3.114.011692DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4065266PMC
June 2014

Gene co-expression modules underlying polymorphic and monomorphic zooids in the colonial hydrozoan, Hydractinia symbiolongicarpus.

Integr Comp Biol 2014 Jul 15;54(2):276-83. Epub 2014 Jun 15.

*Department of Molecular, Cellular and Biomedical Sciences, The University of New Hampshire, Durham, NH 03801, USA; Department of Ecology Evolution and Marine Biology, The University of California at Santa Barbara, Santa Barbara, CA 93106, USA; Department of Entomology, The University of California at Davis, Davis, CA 95616, USA; Department of Evolution and Ecology, Center for Population Biology, The University of California at Davis, Davis, CA 95616, USA.

Advances in sequencing technology have forced a quantitative revolution in Evolutionary Biology. One important feature of this renaissance is that comprehensive genomic resources can be obtained quickly for almost any taxon, thus speeding the development of new model organisms. Here, we analyze 20 RNA-seq libraries from morphologically, sexually, and genetically distinct polyp types from the gonochoristic colonial hydrozoan, Hydractinia symbiolongicarpus (Cnidaria). Analyses of these data using weighted gene co-expression networks highlight deeply conserved genetic elements of animal spermatogenesis and demonstrate the utility of these methods in identifying modules of genes that correlate with different zooid types across various statistical contrasts. RNA-seq data and analytical scripts described here are deposited in publicly available databases.
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http://dx.doi.org/10.1093/icb/icu080DOI Listing
July 2014

Pan-metazoan phylogeny of the DMRT gene family: a framework for functional studies.

Dev Genes Evol 2014 Jun 6;224(3):175-81. Epub 2014 Jun 6.

Center for Population Biology, Department of Evolution and Ecology, University of California, One Shields Ave, Davis, CA, 95616, USA,

The family of Doublesex-Mab-3 Related Transcription factors (DMRTs) includes key regulators of sexual differentiation and neurogenesis. To help understand the functional diversification of this gene family, we examined DMRT gene complements from the whole genome sequences and predicted gene models of 32 animal species representing 12 different phyla and from several non-metazoan outgroups. DMRTs are present in all animals except the sponge Amphimedon queenslandica, but are not found in any of the outgroups, indicating that this gene family is specific to animals and has an ancient pre-eumetazoan origin. Our analyses suggest that DMRT genes diversified independently in bilaterian and non-bilaterian animals. Most clades in the DMRT gene tree, including those containing the well-characterized DMRT1 and doublesex genes, have phylogenetically limited distributions.
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http://dx.doi.org/10.1007/s00427-014-0473-0DOI Listing
June 2014

The making of a pest: the evolution of a fruit-penetrating ovipositor in Drosophila suzukii and related species.

Proc Biol Sci 2014 Apr 26;281(1781):20132840. Epub 2014 Feb 26.

Department of Evolution and Ecology, University of California, , One Shields Avenue, Davis, CA 95616, USA.

Evolutionary innovation can allow a species access to a new ecological niche, potentially reducing competition with closely related species. While the vast majority of Drosophila flies feed on rotting fruit and other decaying matter, and are harmless to human activity, Drosophila suzukii, which has a morphologically modified ovipositor, is capable of colonizing live fruit that is still in the process of ripening, causing massive agricultural damage. Here, we conducted the first comparative analysis of this species and its close relatives, analysing both ovipositor structure and fruit susceptibility. We found that the ovipositor of the species most closely related to D. suzukii, Drosophila subpulchrella, has a similar number of enlarged, evolutionarily derived bristles, but a notably different overall shape. Like D. suzukii, D. subpulchrella flies are capable of puncturing the skin of raspberries and cherries, but we found no evidence that they could penetrate the thicker skin of two varieties of grapes. More distantly related species, one of which has previously been mistaken for D. suzukii, have blunt ovipositors with small bristles. While they did not penetrate fruit skin in any of the assays, they readily colonized fruit interiors where the skin was broken. Our results suggest that considering evolutionary context may be beneficial to the management of invasive species.
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http://dx.doi.org/10.1098/rspb.2013.2840DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3953835PMC
April 2014

Sex-specific repression of dachshund is required for Drosophila sex comb development.

Dev Biol 2014 Feb 19;386(2):440-7. Epub 2013 Dec 19.

Department of Evolution & Ecology, University of California, One Shields Avenue, Davis, CA 95616, USA.

The origin of new morphological structures requires the establishment of new genetic regulatory circuits to control their development, from initial specification to terminal differentiation. The upstream regulatory genes are usually the first to be identified, while the mechanisms that translate novel regulatory information into phenotypic diversity often remain obscure. In particular, elaborate sex-specific structures that have evolved in many animal lineages are inevitably controlled by sex-determining genes, but the genetic basis of sexually dimorphic cell differentiation is rarely understood. In this report, we examine the role of dachshund (dac), a gene with a deeply conserved function in sensory organ and appendage development, in the sex comb, a recently evolved male-specific structure found in some Drosophila species. We show that dac acts during metamorphosis to restrict sex comb development to the appropriate leg region. Localized repression of dac by the sex determination pathway is necessary for male-specific morphogenesis of sex comb bristles. This pupal function of dac is separate from its earlier role in leg patterning, and Dac at this stage is not dependent on the pupal expression of Distalless (Dll), the main regulator of dac during the larval period. Dll acts in the epithelial cells surrounding the sex comb during pupal development to promote sex comb rotation, a complex cellular process driven by coordinated cell rearrangement. Our results show that genes with well-conserved developmental functions can be re-used at later stages in development to regulate more recently evolved traits. This mode of gene co-option may be an important driver of evolutionary innovations.
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http://dx.doi.org/10.1016/j.ydbio.2013.12.017DOI Listing
February 2014

Genomic resources for multiple species in the Drosophila ananassae species group.

Fly (Austin) 2013 Jan-Mar;7(1):47-57

Department of Evolution and Ecology, University of California, Davis, Davis, CA, USA.

The development of genomic resources in non-model taxa is essential for understanding the genetic basis of biological diversity. Although the genomes of many Drosophila species have been sequenced, most of the phenotypic diversity in this genus remains to be explored. To facilitate the genetic analysis of interspecific and intraspecific variation, we have generated new genomic resources for seven species and subspecies in the D. ananassae species subgroup. We have generated large amounts of transcriptome sequence data for D. ercepeae, D. merina, D. bipectinata, D. malerkotliana malerkotliana, D. m. pallens, D. pseudoananassae pseudoananassae, and D. p. nigrens. de novo assembly resulted in contigs covering more than half of the predicted transcriptome and matching an average of 59% of annotated genes in the complete genome of D. ananassae. Most contigs, corresponding to an average of 49% of D. ananassae genes, contain sequence polymorphisms that can be used as genetic markers. Subsets of these markers were validated by genotyping the progeny of inter- and intraspecific crosses. The ananassae subgroup is an excellent model system for examining the molecular basis of speciation and phenotypic evolution. The new genomic resources will facilitate the genetic analysis of inter- and intraspecific differences in this lineage. Transcriptome sequencing provides a simple and cost-effective way to identify molecular markers at nearly single-gene density, and is equally applicable to any non-model taxa.
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http://dx.doi.org/10.4161/fly.22353DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3660750PMC
December 2013

Evolutionary genetics: big effect of a small RNA.

Authors:
Artyom Kopp

Curr Biol 2013 Mar;23(6):R247-9

Department of Ecology and Evolution, Center for Population Biology, University of California Davis, One Shields Ave, Davis, CA 95616, USA.

A new study demonstrates that tissue-specific changes in the expression of a microRNA contribute to morphological variation in nature. This and other examples suggest that the evolution of microRNA-regulated gene networks may follow the same general principles as the more familiar regulatory networks controlled by transcription factors.
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http://dx.doi.org/10.1016/j.cub.2013.02.029DOI Listing
March 2013

Evolutionary genetics: no coming back from neverland.

Authors:
Artyom Kopp

Curr Biol 2012 Dec;22(23):R1004-6

Department of Ecology and Evolution, Center for Population Biology, University of California Davis, One Shields Ave, Davis, CA 95616, USA.

Host-plant specialization plays a key role in insect evolution, but little is known about its molecular basis. A new paper shows that a cactus-feeding fly became restricted to its host by changes in an enzyme that converts dietary sterols into essential hormones.
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http://dx.doi.org/10.1016/j.cub.2012.10.040DOI Listing
December 2012

Many ways to make a novel structure: a new mode of sex comb development in Drosophilidae.

Evol Dev 2012 Nov-Dec;14(6):476-83

Department of Evolution and Ecology, University of California, Davis, CA 95616, USA.

On macroevolutionary time scales, the same genes can regulate the development of homologous structures through strikingly different cellular processes. Comparing the development of similar morphological traits in closely related species may help elucidate the evolutionary dissociation between pattern formation and morphogenesis. We address this question by focusing on the interspecific differences in sex comb development in Drosophilids. The sex comb is a recently evolved, male-specific structure composed of modified bristles. Previous work in the obscura and melanogaster species groups (Old World Sophophora) has identified two distinct cellular mechanisms that give rise to nearly identical adult morphologies. Here, we describe sex comb development in a species from a more distantly related lineage, the genus Lordiphosa. Although the expression of key regulatory genes is largely conserved in both clades, the cell behaviors responsible for sex comb formation show major differences between Old World Sophophora and Lordiphosa. We suggest that the many-to-one mapping between development and adult phenotype increases the potential for evolutionary innovations.
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http://dx.doi.org/10.1111/ede.12001DOI Listing
March 2013

Genetic basis of a violation of Dollo's Law: re-evolution of rotating sex combs in Drosophila bipectinata.

Genetics 2012 Dec 19;192(4):1465-75. Epub 2012 Oct 19.

Department of Evolution and Ecology, University of California, Davis, CA 95616, USA.

Phylogenetic analyses suggest that violations of "Dollo's law"--that is, re-evolution of lost complex structures--do occur, albeit infrequently. However, the genetic basis of such reversals has not been examined. Here, we address this question using the Drosophila sex comb, a recently evolved, male-specific morphological structure composed of modified bristles. In some species, sex comb development involves only the modification of individual bristles, while other species have more complex "rotated" sex combs that are shaped by coordinated migration of epithelial tissues. Rotated sex combs were lost in the ananassae species subgroup and subsequently re-evolved, ∼12 million years later, in Drosophila bipectinata and its sibling species. We examine the genetic basis of the differences in sex comb morphology between D. bipectinata and D. malerkotliana, a closely related species with a much simpler sex comb representing the ancestral condition. QTL mapping reveals that >50% of this difference is controlled by one chromosomal inversion that covers ∼5% of the genome. Several other, larger inversions do not contribute appreciably to the phenotype. This genetic architecture suggests that rotating sex combs may have re-evolved through changes in relatively few genes. We discuss potential developmental mechanisms that may allow lost complex structures to be regained.
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http://dx.doi.org/10.1534/genetics.112.145524DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3512151PMC
December 2012

Drosophila sex combs as a model of evolutionary innovations.

Authors:
Artyom Kopp

Evol Dev 2011 Nov-Dec;13(6):504-22

Department of Evolution and Ecology, University of California - Davis, Davis, CA 95616, USA.

The diversity of animal and plant forms is shaped by nested evolutionary innovations. Understanding the genetic and molecular changes responsible for these innovations is therefore one of the key goals of evolutionary biology. From the genetic point of view, the origin of novel traits implies the origin of new regulatory pathways to control their development. To understand how these new pathways are assembled in the course of evolution, we need model systems that combine relatively recent innovations with a powerful set of genetic and molecular tools. One such model is provided by the Drosophila sex comb-a male-specific morphological structure that evolved in a relatively small lineage related to the model species D. melanogaster. Our extensive knowledge of sex comb development in D. melanogaster provides the basis for investigating the genetic changes responsible for sex comb origin and diversification. At the same time, sex combs can change on microevolutionary timescales and differ spectacularly among closely related species, providing opportunities for direct genetic analysis and for integrating developmental and population-genetic approaches. Sex comb evolution is associated with the origin of novel interactions between Hox and sex determination genes. Activity of the sex determination pathway was brought under the control of the Hox code to become segment-specific, while Hox gene expression became sexually dimorphic. At the same time, both Hox and sex determination genes were integrated into the intrasegmental spatial patterning network, and acquired new joint downstream targets. Phylogenetic analysis shows that similar sex comb morphologies evolved independently in different lineages. Convergent evolution at the phenotypic level reflects convergent changes in the expression of Hox and sex determination genes, involving both independent gains and losses of regulatory interactions. However, the downstream cell-differentiation programs have diverged between species, and in some lineages, similar adult morphologies are produced by different morphogenetic mechanisms. These features make the sex comb an excellent model for examining not only the genetic changes responsible for its evolution, but also the cellular processes that translate DNA sequence changes into morphological diversity. The origin and diversification of sex combs provides insights into the roles of modularity, cooption, and regulatory changes in evolutionary innovations, and can serve as a model for understanding the origin of the more drastic novelties that define higher order taxa.
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http://dx.doi.org/10.1111/j.1525-142X.2011.00507.xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3462374PMC
January 2013

Yeast communities of diverse Drosophila species: comparison of two symbiont groups in the same hosts.

Appl Environ Microbiol 2012 Oct 10;78(20):7327-36. Epub 2012 Aug 10.

Department of Evolution and Ecology and Center for Population Biology, University of California Davis, Davis, California, USA.

The combination of ecological diversity with genetic and experimental tractability makes Drosophila a powerful model for the study of animal-associated microbial communities. Despite the known importance of yeasts in Drosophila physiology, behavior, and fitness, most recent work has focused on Drosophila-bacterial interactions. In order to get a more complete understanding of the Drosophila microbiome, we characterized the yeast communities associated with different Drosophila species collected around the world. We focused on the phylum Ascomycota because it constitutes the vast majority of the Drosophila-associated yeasts. Our sampling strategy allowed us to compare the distribution and structure of the yeast and bacterial communities in the same host populations. We show that yeast communities are dominated by a small number of abundant taxa, that the same yeast lineages are associated with different host species and populations, and that host diet has a greater effect than host species on yeast community composition. These patterns closely parallel those observed in Drosophila bacterial communities. However, we do not detect a significant correlation between the yeast and bacterial communities of the same host populations. Comparative analysis of different symbiont groups provides a more comprehensive picture of host-microbe interactions. Future work on the role of symbiont communities in animal physiology, ecological adaptation, and evolution would benefit from a similarly holistic approach.
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http://dx.doi.org/10.1128/AEM.01741-12DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3457106PMC
October 2012

Mechanisms of speciation.

Int J Evol Biol 2012 9;2012:820358. Epub 2012 May 9.

Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba 305-8572, Japan.

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http://dx.doi.org/10.1155/2012/820358DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3357519PMC
August 2012

Unraveling the thread of nature's tapestry: the genetics of diversity and convergence in animal pigmentation.

Pigment Cell Melanoma Res 2012 Jul;25(4):411-33

FAS Center for Systems Biology, Harvard University, Cambridge, MA, USA.

Animals display incredibly diverse color patterns yet little is known about the underlying genetic basis of these phenotypes. However, emerging results are reshaping our view of how the process of phenotypic evolution occurs. Here, we outline recent research from three particularly active areas of investigation: melanin pigmentation in Drosophila, wing patterning in butterflies, and pigment variation in lizards. For each system, we highlight (i) the function and evolution of color variation, (ii) various approaches that have been used to explore the genetic basis of pigment variation, and (iii) conclusions regarding the genetic basis of convergent evolution which have emerged from comparative analyses. Results from these studies indicate that natural variation in pigmentation is a particularly powerful tool to examine the molecular basis of evolution, especially with regard to convergent or parallel evolution. Comparison of these systems also reveals that the molecular basis of convergent evolution is heterogeneous, sometimes involving conserved mechanisms and sometimes not. In the near future, additional work in other emerging systems will substantially expand the scope of available comparisons.
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http://dx.doi.org/10.1111/j.1755-148X.2012.01014.xDOI Listing
July 2012