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. 2016 Sep 22;17(1):192.
doi: 10.1186/s13059-016-1049-2.

The whole genome sequence of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), reveals insights into the biology and adaptive evolution of a highly invasive pest species

Alexie Papanicolaou  1 , Marc F Schetelig  2 , Peter Arensburger  3 , Peter W Atkinson  4   5 , Joshua B Benoit  6 , Kostas Bourtzis  7   8 , Pedro Castañera  9 , John P Cavanaugh  6 , Hsu Chao  10 , Christopher Childers  11 , Ingrid Curril  12 , Huyen Dinh  10 , HarshaVardhan Doddapaneni  10 , Amanda Dolan  13 , Shannon Dugan  10 , Markus Friedrich  14 , Giuliano Gasperi  15 , Scott Geib  16 , Georgios Georgakilas  17 , Richard A Gibbs  10 , Sarah D Giers  18 , Ludvik M Gomulski  15 , Miguel González-Guzmán  9 , Ana Guillem-Amat  9 , Yi Han  10 , Artemis G Hatzigeorgiou  17 , Pedro Hernández-Crespo  9 , Daniel S T Hughes  10 , Jeffery W Jones  19 , Dimitra Karagkouni  17 , Panagiota Koskinioti  20 , Sandra L Lee  10 , Anna R Malacrida  15 , Mosè Manni  15 , Kostas Mathiopoulos  20 , Angela Meccariello  21 , Monica Munoz-Torres, Shwetha C Murali  10 , Terence D Murphy  22 , Donna M Muzny  10 , Georg Oberhofer  12 , Félix Ortego  9 , Maria D Paraskevopoulou  17 , Monica Poelchau  11 , Jiaxin Qu  10 , Martin Reczko  23 , Hugh M Robertson  18 , Andrew J Rosendale  6 , Andrew E Rosselot  6 , Giuseppe Saccone  21 , Marco Salvemini  21 , Grazia Savini  15 , Patrick Schreiner  5 , Francesca Scolari  15 , Paolo Siciliano  15 , Sheina B Sim  16 , George Tsiamis  8 , Enric Ureña  9 , Ioannis S Vlachos  17 , John H Werren  13 , Ernst A Wimmer  12 , Kim C Worley  10 , Antigone Zacharopoulou  24 , Stephen Richards  10 , Alfred M Handler  25
Affiliations

The whole genome sequence of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), reveals insights into the biology and adaptive evolution of a highly invasive pest species

Alexie Papanicolaou et al. Genome Biol. .

Erratum in

  • Erratum to: The whole genome sequence of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), reveals insights into the biology and adaptive evolution of a highly invasive pest species.
    Papanicolaou A, Schetelig MF, Arensburger P, Atkinson PW, Benoit JB, Bourtzis K, Castañera P, Cavanaugh JP, Chao H, Childers C, Curril I, Dinh H, Doddapaneni H, Dolan A, Dugan S, Friedrich M, Gasperi G, Geib S, Georgakilas G, Gibbs RA, Giers SD, Gomulski LM, González-Guzmán M, Guillem-Amat A, Han Y, Hatzigeorgiou AG, Hernández-Crespo P, Hughes DS, Jones JW, Karagkouni D, Koskinioti P, Lee SL, Malacrida AR, Manni M, Mathiopoulos K, Meccariello A, Munoz-Torres M, Murali SC, Murphy TD, Muzny DM, Oberhofer G, Ortego F, Paraskevopoulou MD, Poelchau M, Qu J, Reczko M, Robertson HM, Rosendale AJ, Rosselot AE, Saccone G, Salvemini M, Savini G, Schreiner P, Scolari F, Siciliano P, Sim SB, Tsiamis G, Ureña E, S Vlachos I, Werren JH, Wimmer EA, Worley KC, Zacharopoulou A, Richards S, Handler AM. Papanicolaou A, et al. Genome Biol. 2017 Jan 18;18(1):11. doi: 10.1186/s13059-017-1155-9. Genome Biol. 2017. PMID: 28100280 Free PMC article. No abstract available.

Abstract

Background: The Mediterranean fruit fly (medfly), Ceratitis capitata, is a major destructive insect pest due to its broad host range, which includes hundreds of fruits and vegetables. It exhibits a unique ability to invade and adapt to ecological niches throughout tropical and subtropical regions of the world, though medfly infestations have been prevented and controlled by the sterile insect technique (SIT) as part of integrated pest management programs (IPMs). The genetic analysis and manipulation of medfly has been subject to intensive study in an effort to improve SIT efficacy and other aspects of IPM control.

Results: The 479 Mb medfly genome is sequenced from adult flies from lines inbred for 20 generations. A high-quality assembly is achieved having a contig N50 of 45.7 kb and scaffold N50 of 4.06 Mb. In-depth curation of more than 1800 messenger RNAs shows specific gene expansions that can be related to invasiveness and host adaptation, including gene families for chemoreception, toxin and insecticide metabolism, cuticle proteins, opsins, and aquaporins. We identify genes relevant to IPM control, including those required to improve SIT.

Conclusions: The medfly genome sequence provides critical insights into the biology of one of the most serious and widespread agricultural pests. This knowledge should significantly advance the means of controlling the size and invasive potential of medfly populations. Its close relationship to Drosophila, and other insect species important to agriculture and human health, will further comparative functional and structural studies of insect genomes that should broaden our understanding of gene family evolution.

Keywords: Chromosomal synteny; Gene family evolution; Insect adaptation; Insect invasiveness; Insect orthology; Medfly genome; Medfly integrated pest management (IPM); Tephritid genomics.

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Figures

Fig. 1
Fig. 1
Genome-wide phylogenomics and orthology. The phylogenetic relationship of C. capitata and 13 species in Arthropoda was estimated using a maximum likelihood analysis of a concatenation of 2591 single-copy orthologous protein sequences, 1000 bootstrap replicates, and rooted with D. pulex. The scale bar represents 0.1 amino acid substitution per site and the asterisks represent nodes with a bootstrap value of 100. Horizontal bars for each species show the absolute number of proteins that are: single-copy orthologs in all species, present in all species (not necessarily in single-copy), present in the majority of species in the analysis, present in a minority of the species (patchy distribution) in the analysis, and unique to the species. Species/strain designations are: Acyrthosiphon pisum (AcP), Aedes aegypti (strain Liverpool) (AeA), Anopheles gambiae (strain PEST) (AnG), Apis mellifera (ApM), Bombyx mori (BoM), Ceratitis capitata (CeC), Cimex lectularius (CiL), Culex quinquefasciatus (strain Johannesburg) (CuQ), Daphnia pulex (DaP), Drosophila melanogaster (DrM), Manduca sexta (MaS), Musca domestica (MuD), Pediculus humanus (PeH), Solenopsis invicta (SoI), and Tribolium castaneum (TrC)
Fig. 2
Fig. 2
C. capitata genome scaffold map based on scaffold linkage of annotated genes and microsatellite (Medflymic) sequences previously localized to map banding positions by in situ hybridization to autosomal polytene chromosomes (chromosomes 2 to 6). The larval salivary gland polytene chromosome map [193] presented includes left (L) and right (R) autosomal chromosome arms linked at a centromeric region (K). Arrows with adjacent scaffold numbers point to mapped loci positions of designated genes/microsatellites, with bracketed positions used for less precise mapping. See Additional file 2: Table S6 for sequence and scaffold accession numbers and sizes, in addition to map positions for sex-linked (chromosome 1; X and Y) genes/sequences mapped to undefined loci on mitotic non-polytenized chromosome spreads [20, 21]
Fig. 3
Fig. 3
In situ hybridization mapping of piggyBac transformation vector insertions on chromosome 5 having the D53 inversion used in the VIENNA-8 tsl genetic sexing strain. Top: a schematic of chromosome 5 showing the piggyBac vector insertion sites along with other mapped genes and the D53 inversion breakpoints. Bottom: images of the yellow fluorescent-tagged hybridization site loci (arrows) on third larval instar salivary gland polytene chromosome spreads
Fig. 4
Fig. 4
Comparison of gene numbers for odorant-binding proteins (OBPs), odorant receptors (ORs), gustatory receptors (GRs), and ionotrophic receptors (IRs) in C. capitata, D. melanogaster, and M. domestica. Gene numbers provided above each bar
Fig. 5
Fig. 5
Phylogenetic relationships of OR proteins from C. capitata, D. melanogaster, and M. domestica. The unrooted maximum likelihood (log likelihood = –140908) tree was inferred using the Le and Gascuel model [208] with a discrete Gamma distribution and some invariable sites. Bootstrap values greater than 50 % (1000 replications) are shown. Suffixes after the gene/protein names are: -CTE, C-terminus missing; -PSE, pseudogene
Fig. 6
Fig. 6
Phylogenetic tree of C. capitata GR proteins with those from D. melanogaster and M. domestica. The maximum likelihood tree was rooted by assigning the carbon dioxide and sugar receptor subfamilies as the outgroup. Clades discussed in the text are indicated on the outer edge
Fig. 7
Fig. 7
Comparison of predicted AQP amino acid sequences from C. capitata and other indicated Diptera. The neighbor-joining tree was produced using MEGA6 using Dayhoff Model and pairwise matching; branch values indicate support following 3000 bootstraps with values below 20 % omitted. Classification is based upon Finn et al., Benoit et al., and Fabrick et al. [87, 88, 226]. Drip Drosophila integral protein, Prip Pyrocoelia rufa integral protein, Eglp entomoglyceroporin, AQP aquaporin. Unorthodox AQPs are not included in this analysis
Fig. 8
Fig. 8
Bootstrap PhyML tree (http://phylogeny.lirmm.fr/) performed with protein sequences of the CYP3 and mitochondrial clans of cytochrome P450 genes found in the genome of C. capitata (red) and D. melanogaster (blue). Expanded CYP6 and CYP12 subfamilies are highlighted. Branch length scale indicates average residue substitutions per site
Fig. 9
Fig. 9
Bootstrap PhyML tree of C. capitata (red) and D. melanogaster (blue) esterase protein sequences (http://phylogeny.lirmm.fr/). Clades are indicated by letters, A–N. Branch length scale indicates average residue substitutions per site
Fig. 10
Fig. 10
Phylogenetic tree demonstrating relationships of Tweedle proteins from Ceratitis capitata (Cc), Drosophila melanogaster (Dm), Musca domestica (Md), Anopheles gambiae (Ag), Aedes aegypti (Aa), Glossina morsitans (Gm), Culex quinquefasciatus (Cq), Cimex lectularius (Cl), Rhodnius prolixus (Rp), Tribolium castaneum (Tc), Pediculus humanus (Ph), and Acyrthosiphon pisum (Ap). The tree was constructed using the neighbor-joining method in MEGA6; Poisson correction and bootstrap replicates (2000 replicates) were used
Fig. 11
Fig. 11
Pro-apoptotic RHG gene group syntenic relationships and relative distances in D. melanogaster (top) and C. capitata (bottom). A comparison between the RHG regions, including the hid, grim, rpr (reaper), and skl (sickle) genes, located on chromosome 3L (75C) in D. melanogaster and on chromosome 6R (scaffold 2; NW_004523691) in C. capitata, reveals a similar organization of genes in the two species. The RHG region in C. capitata is 2.9-fold larger relative to D. melanogaster, which correlates approximately to the relative total genome size of the two species
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