publication . Article . 2016

Anchored enrichment dataset for true flies (order Diptera) reveals insights into the phylogeny of flower flies (family Syrphidae)

Young, Andrew Donovan; Lemmon, Alan R.; Skevington, Jeffrey H.; Mengual, Ximo; Ståhls, Gunilla; Reemer, Menno; Jordaens, Kurt; Kelso, Scott; Lemmon, Emily Moriarty; Hauser, Martin; ...
Open Access English
  • Published: 29 Jun 2016
  • Country: Finland
Abstract
Background Anchored hybrid enrichment is a form of next-generation sequencing that uses oligonucleotide probes to target conserved regions of the genome flanked by less conserved regions in order to acquire data useful for phylogenetic inference from a broad range of taxa. Once a probe kit is developed, anchored hybrid enrichment is superior to traditional PCR-based Sanger sequencing in terms of both the amount of genomic data that can be recovered and effective cost. Due to their incredibly diverse nature, importance as pollinators, and historical instability with regard to subfamilial and tribal classification, Syrphidae (flower flies or hoverflies) are an ideal candidate for anchored hybrid enrichment-based phylogenetics, especially since recent molecular phylogenies of the syrphids using only a few markers have resulted in highly unresolved topologies. Over 6200 syrphids are currently known and uncovering their phylogeny will help us to understand how these species have diversified, providing insight into an array of ecological processes, from the development of adult mimicry, the origin of adult migration, to pollination patterns and the evolution of larval resource utilization. Results We present the first use of anchored hybrid enrichment in insect phylogenetics on a dataset containing 30 flower fly species from across all four subfamilies and 11 tribes out of 15. To produce a phylogenetic hypothesis, 559 loci were sampled to produce a final dataset containing 217,702 sites. We recovered a well resolved topology with bootstrap support values that were almost universally >95 %. The subfamily Eristalinae is recovered as paraphyletic, with the strongest support for this hypothesis to date. The ant predators in the Microdontinae are sister to all other syrphids. Syrphinae and Pipizinae are monophyletic and sister to each other. Larval predation on soft-bodied hemipterans evolved only once in this family. Conclusions Anchored hybrid enrichment was successful in producing a robustly supported phylogenetic hypothesis for the syrphids. Subfamilial reconstruction is concordant with recent phylogenetic hypotheses, but with much higher support values. With the newly designed probe kit this analysis could be rapidly expanded with further sampling, opening the door to more comprehensive analyses targeting problem areas in syrphid phylogenetics and ecology. Electronic supplementary material The online version of this article (doi:10.1186/s12862-016-0714-0) contains supplementary material, which is available to authorized users.
Persistent Identifiers
Fields of Science and Technology classification (FOS)
01 natural sciences, 0106 biological sciences, 010603 evolutionary biology, 03 medical and health sciences, 0301 basic medicine, 030104 developmental biology
Subjects
free text keywords: Flower flies ; Hybrid enrichment ; Syrphinae ; Anchored phylogenetics ; Microdontinae ; Hoverflies ; Eristalinae ; Pipizinae, Ecology, Evolution, Behavior and Systematics, Anchored phylogenetics, Hybrid enrichment, Syrphinae, Microdontinae, Eristalinae, Pipizinae, Flower flies, Hoverflies, OBLIGATE PREDATOR, CHEMICAL MIMICRY, POLLINATION, SYSTEMATICS, EVOLUTION, BIOLOGY, HISTORY, LARVAL, CLASSIFICATION, 1181 Ecology, evolutionary biology, Research Article, Phylogenetics, Microdontinae, biology.organism_classification, biology, Taxon, Monophyly, Evolutionary biology, Eristalinae, Paraphyly, Zoology, Systematics, Phylogenetic tree
Communities
  • Digital Humanities and Cultural Heritage
  • Social Science and Humanities
Funded by
NSERC
Project
  • Funder: Natural Sciences and Engineering Research Council of Canada (NSERC)
,
NSF| I-Corps: Anchored Hybrid Enrichment
Project
  • Funder: National Science Foundation (NSF)
  • Project Code: 1313554
  • Funding stream: Directorate for Engineering | Division of Industrial Innovation & Partnerships
,
NSF| Beyond Drosophila: Comparative transcriptomics of schizophoran flies to resolve a rapid radiation
Project
  • Funder: National Science Foundation (NSF)
  • Project Code: 1257960
  • Funding stream: Directorate for Biological Sciences | Division of Environmental Biology
91 references, page 1 of 7

1. Beutel RG, Friedrich F, Hörnschemeyer T, Pohl H, Hünefeld F, Beckmann F, Meier R, Misof B, Whiting MF, Vilhelmsen L. Morphological and molecular evidence converge upon a robust phylogeny of the megadiverse Holometabola. Cladistics. 2010;26:1-15.

2. Misof B, Liu S, Meusemann K, Peters RS, Donath A, Mayer C, Frandsen PB, Ware J, Flouri T, Beutel RG. Phylogenomics resolves the timing and pattern of insect evolution. Science. 2014;346(6210):763-7.

3. Hackett SJ, Kimball RT, Reddy S, Bowie RC, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han K-L, Harshman J. A phylogenomic study of birds reveals their evolutionary history. Science. 2008;320(5884):1763-8.

4. McCormack JE, Harvey MG, Faircloth BC, Crawford NG, Glenn TC, Brumfield RT. A phylogeny of birds based on over 1,500 loci collected by target enrichment and high-throughput sequencing. PLoS One. 2013;8(1), e54848.

5. Prum RO, Berv JS, Dornburg A, Field DJ, Townsend JP, Lemmon EM, Lemmon AR. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature. 2015;526:569-73. [OpenAIRE]

6. Meredith RW, Janečka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Simão TL, Stadler T. Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification. Science. 2011;334(6055):521-4.

7. Pyron RA, Burbrink FT, Wiens JJ. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol Biol. 2013;13(1):93. [OpenAIRE]

8. Glenn TC. Field guide to next‐generation DNA sequencers. Mol Ecol Resour. 2011;11(5):759-69.

9. Albert TJ, Molla MN, Muzny DM, Nazareth L, Wheeler D, Song X, Richmond TA, Middle CM, Rodesch MJ, Packard CJ. Direct selection of human genomic loci by microarray hybridization. Nat Methods. 2007;4(11):903-5.

10. Gnirke A, Melnikov A, Maguire J, Rogov P, LeProust EM, Brockman W, Fennell T, Giannoukos G, Fisher S, Russ C. Solution hybrid selection with ultra-long oligonucleotides for massively parallel targeted sequencing. Nat Biotechnol. 2009;27(2):182-9.

11. Bamshad MJ, Ng SB, Bigham AW, Tabor HK, Emond MJ, Nickerson DA, Shendure J. Exome sequencing as a tool for Mendelian disease gene discovery. Nat Rev Genet. 2011;12(11):745-55. [OpenAIRE]

12. Faircloth BC, McCormack JE, Crawford NG, Harvey MG, Brumfield RT, Glenn TC. Ultraconserved elements anchor thousands of genetic markers spanning multiple evolutionary timescales. Syst Biol. 2012;61(5):717-26.

13. Lemmon AR, Emme SA, Lemmon EM. Anchored hybrid enrichment for massively high-throughput phylogenomics. Syst Biol. 2012;61(5):727-44. [OpenAIRE]

14. Eytan RI, Evans BR, Dornburg A, Lemmon AR, Lemmon EM, Wainwright PC, Near TJ. Are 100 enough? Inferring acanthomorph teleost phylogeny using Anchored Hybrid Enrichment. BMC Evol Biol. 2015;15(1):1.

15. Lemmon EM, Lemmon AR. High-throughput genomic data in systematics and phylogenetics. Annu Rev Ecol Evol Syst. 2013;44:99-121. [OpenAIRE]

91 references, page 1 of 7
Abstract
Background Anchored hybrid enrichment is a form of next-generation sequencing that uses oligonucleotide probes to target conserved regions of the genome flanked by less conserved regions in order to acquire data useful for phylogenetic inference from a broad range of taxa. Once a probe kit is developed, anchored hybrid enrichment is superior to traditional PCR-based Sanger sequencing in terms of both the amount of genomic data that can be recovered and effective cost. Due to their incredibly diverse nature, importance as pollinators, and historical instability with regard to subfamilial and tribal classification, Syrphidae (flower flies or hoverflies) are an ideal candidate for anchored hybrid enrichment-based phylogenetics, especially since recent molecular phylogenies of the syrphids using only a few markers have resulted in highly unresolved topologies. Over 6200 syrphids are currently known and uncovering their phylogeny will help us to understand how these species have diversified, providing insight into an array of ecological processes, from the development of adult mimicry, the origin of adult migration, to pollination patterns and the evolution of larval resource utilization. Results We present the first use of anchored hybrid enrichment in insect phylogenetics on a dataset containing 30 flower fly species from across all four subfamilies and 11 tribes out of 15. To produce a phylogenetic hypothesis, 559 loci were sampled to produce a final dataset containing 217,702 sites. We recovered a well resolved topology with bootstrap support values that were almost universally >95 %. The subfamily Eristalinae is recovered as paraphyletic, with the strongest support for this hypothesis to date. The ant predators in the Microdontinae are sister to all other syrphids. Syrphinae and Pipizinae are monophyletic and sister to each other. Larval predation on soft-bodied hemipterans evolved only once in this family. Conclusions Anchored hybrid enrichment was successful in producing a robustly supported phylogenetic hypothesis for the syrphids. Subfamilial reconstruction is concordant with recent phylogenetic hypotheses, but with much higher support values. With the newly designed probe kit this analysis could be rapidly expanded with further sampling, opening the door to more comprehensive analyses targeting problem areas in syrphid phylogenetics and ecology. Electronic supplementary material The online version of this article (doi:10.1186/s12862-016-0714-0) contains supplementary material, which is available to authorized users.
Persistent Identifiers
Fields of Science and Technology classification (FOS)
01 natural sciences, 0106 biological sciences, 010603 evolutionary biology, 03 medical and health sciences, 0301 basic medicine, 030104 developmental biology
Subjects
free text keywords: Flower flies ; Hybrid enrichment ; Syrphinae ; Anchored phylogenetics ; Microdontinae ; Hoverflies ; Eristalinae ; Pipizinae, Ecology, Evolution, Behavior and Systematics, Anchored phylogenetics, Hybrid enrichment, Syrphinae, Microdontinae, Eristalinae, Pipizinae, Flower flies, Hoverflies, OBLIGATE PREDATOR, CHEMICAL MIMICRY, POLLINATION, SYSTEMATICS, EVOLUTION, BIOLOGY, HISTORY, LARVAL, CLASSIFICATION, 1181 Ecology, evolutionary biology, Research Article, Phylogenetics, Microdontinae, biology.organism_classification, biology, Taxon, Monophyly, Evolutionary biology, Eristalinae, Paraphyly, Zoology, Systematics, Phylogenetic tree
Communities
  • Digital Humanities and Cultural Heritage
  • Social Science and Humanities
Funded by
NSERC
Project
  • Funder: Natural Sciences and Engineering Research Council of Canada (NSERC)
,
NSF| I-Corps: Anchored Hybrid Enrichment
Project
  • Funder: National Science Foundation (NSF)
  • Project Code: 1313554
  • Funding stream: Directorate for Engineering | Division of Industrial Innovation & Partnerships
,
NSF| Beyond Drosophila: Comparative transcriptomics of schizophoran flies to resolve a rapid radiation
Project
  • Funder: National Science Foundation (NSF)
  • Project Code: 1257960
  • Funding stream: Directorate for Biological Sciences | Division of Environmental Biology
91 references, page 1 of 7

1. Beutel RG, Friedrich F, Hörnschemeyer T, Pohl H, Hünefeld F, Beckmann F, Meier R, Misof B, Whiting MF, Vilhelmsen L. Morphological and molecular evidence converge upon a robust phylogeny of the megadiverse Holometabola. Cladistics. 2010;26:1-15.

2. Misof B, Liu S, Meusemann K, Peters RS, Donath A, Mayer C, Frandsen PB, Ware J, Flouri T, Beutel RG. Phylogenomics resolves the timing and pattern of insect evolution. Science. 2014;346(6210):763-7.

3. Hackett SJ, Kimball RT, Reddy S, Bowie RC, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han K-L, Harshman J. A phylogenomic study of birds reveals their evolutionary history. Science. 2008;320(5884):1763-8.

4. McCormack JE, Harvey MG, Faircloth BC, Crawford NG, Glenn TC, Brumfield RT. A phylogeny of birds based on over 1,500 loci collected by target enrichment and high-throughput sequencing. PLoS One. 2013;8(1), e54848.

5. Prum RO, Berv JS, Dornburg A, Field DJ, Townsend JP, Lemmon EM, Lemmon AR. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature. 2015;526:569-73. [OpenAIRE]

6. Meredith RW, Janečka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Simão TL, Stadler T. Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification. Science. 2011;334(6055):521-4.

7. Pyron RA, Burbrink FT, Wiens JJ. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol Biol. 2013;13(1):93. [OpenAIRE]

8. Glenn TC. Field guide to next‐generation DNA sequencers. Mol Ecol Resour. 2011;11(5):759-69.

9. Albert TJ, Molla MN, Muzny DM, Nazareth L, Wheeler D, Song X, Richmond TA, Middle CM, Rodesch MJ, Packard CJ. Direct selection of human genomic loci by microarray hybridization. Nat Methods. 2007;4(11):903-5.

10. Gnirke A, Melnikov A, Maguire J, Rogov P, LeProust EM, Brockman W, Fennell T, Giannoukos G, Fisher S, Russ C. Solution hybrid selection with ultra-long oligonucleotides for massively parallel targeted sequencing. Nat Biotechnol. 2009;27(2):182-9.

11. Bamshad MJ, Ng SB, Bigham AW, Tabor HK, Emond MJ, Nickerson DA, Shendure J. Exome sequencing as a tool for Mendelian disease gene discovery. Nat Rev Genet. 2011;12(11):745-55. [OpenAIRE]

12. Faircloth BC, McCormack JE, Crawford NG, Harvey MG, Brumfield RT, Glenn TC. Ultraconserved elements anchor thousands of genetic markers spanning multiple evolutionary timescales. Syst Biol. 2012;61(5):717-26.

13. Lemmon AR, Emme SA, Lemmon EM. Anchored hybrid enrichment for massively high-throughput phylogenomics. Syst Biol. 2012;61(5):727-44. [OpenAIRE]

14. Eytan RI, Evans BR, Dornburg A, Lemmon AR, Lemmon EM, Wainwright PC, Near TJ. Are 100 enough? Inferring acanthomorph teleost phylogeny using Anchored Hybrid Enrichment. BMC Evol Biol. 2015;15(1):1.

15. Lemmon EM, Lemmon AR. High-throughput genomic data in systematics and phylogenetics. Annu Rev Ecol Evol Syst. 2013;44:99-121. [OpenAIRE]

91 references, page 1 of 7
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