Episodic radiations in the fly tree of life

Brian M. Wiegmann; Michelle D. Trautwein; Isaac S. Winkler; Norman B. Barr; Jung-Wook Kim; Christine Lambkin; Matthew A. Bertone; Brian K. Cassel; Keith M. Bayless; Alysha M. Heimberg; Benjamin M. Wheeler; Kevin J. Peterson; Thomas Pape; Bradley J. Sinclair; Jeffrey H. Skevington; Vladimir Blagoderov; Jason Caravas; Sujatha Narayanan Kutty; Urs Schmidt-Ott; Gail E. Kampmeier; F. Christian Thompson; David A. Grimaldi; Andrew T. Beckenbach; Gregory W. Courtney; Markus Friedrich; Rudolf Meier; David K. Yeates

doi:10.1073/pnas.1012675108

Episodic radiations in the fly tree of life

Brian M. Wiegmann, Michelle D. Trautwein, Isaac S. Winkler, Norman B. Barr, Jung-Wook Kim, Christine Lambkin, Matthew A. Bertone, Brian K. Cassel, Keith M. Bayless, Alysha M. Heimberg, Benjamin M. Wheeler, Kevin J. Peterson, Thomas Pape, Bradley J. Sinclair, Jeffrey H. Skevington, Vladimir Blagoderov, Jason Caravas, Sujatha Narayanan Kutty, Urs Schmidt-Ott, Gail E. KampmeierF. Christian Thompson, David A. Grimaldi, Andrew T. Beckenbach, Gregory W. Courtney, Markus Friedrich, Rudolf Meier, David K. Yeates

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Abstract

Flies are one of four superradiations of insects (along with beetles, wasps, and moths) that account for the majority of animal life on Earth. Diptera includes species known for their ubiquity (Musca domestica house fly), their role as pests (Anopheles gambiae malaria mosquito), and their value as model organisms across the biological sciences (Drosophila melanogaster). A resolved phylogeny for flies provides a framework for genomic, developmental, and evolutionary studies by facilitating comparisons across model organisms, yet recent research has suggested that fly relationships have been obscured by multiple episodes of rapid diversification. We provide a phylogenomic estimate of fly relationships based on molecules and morphology from 149 of 157 families, including 30 kb from 14 nuclear loci and complete mitochondrial genomes combined with 371 morphological characters. Multiple analyses show support for traditional groups (Brachycera, Cyclorrhapha, and Schizophora) and corroborate contentious findings, such as the anomalous Deuterophlebiidae as the sister group to all remaining Diptera. Our findings reveal that the closest relatives of the Drosophilidae are highly modified parasites (including the wingless Braulidae) of bees and other insects. Furthermore, we use micro-RNAs to resolve a node with implications for the evolution of embryonic development in Diptera. We demonstrate that flies experienced three episodes of rapid radiation—lower Diptera (220 Ma), lower Brachycera (180 Ma), and Schizophora (65 Ma)—and a number of life history transitions to hematophagy, phytophagy, and parasitism in the history of fly evolution over 260 million y.

Original language	English
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	108
Issue number	14
Pages (from-to)	5690-5695
Number of pages	6
ISSN	0027-8424
DOIs	https://doi.org/10.1073/pnas.1012675108
Publication status	Published - 5 Apr 2011

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Wiegmann, B. M., Trautwein, M. D., Winkler, I. S., Barr, N. B., Kim, J-W., Lambkin, C., Bertone, M. A., Cassel, B. K., Bayless, K. M., Heimberg, A. M., Wheeler, B. M., Peterson, K. J., Pape, T., Sinclair, B. J., Skevington, J. H., Blagoderov, V., Caravas, J., Kutty, S. N., Schmidt-Ott, U., ... Yeates, D. K. (2011). Episodic radiations in the fly tree of life. Proceedings of the National Academy of Sciences of the United States of America, 108(14), 5690-5695. https://doi.org/10.1073/pnas.1012675108

Wiegmann, BM, Trautwein, MD, Winkler, IS, Barr, NB, Kim, J-W, Lambkin, C, Bertone, MA, Cassel, BK, Bayless, KM, Heimberg, AM, Wheeler, BM, Peterson, KJ, Pape, T, Sinclair, BJ, Skevington, JH, Blagoderov, V, Caravas, J, Kutty, SN, Schmidt-Ott, U, Kampmeier, GE, Thompson, FC, Grimaldi, DA, Beckenbach, AT, Courtney, GW, Friedrich, M, Meier, R & Yeates, DK 2011, 'Episodic radiations in the fly tree of life', Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 14, pp. 5690-5695. https://doi.org/10.1073/pnas.1012675108

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title = "Episodic radiations in the fly tree of life",

abstract = "Flies are one of four superradiations of insects (along with beetles, wasps, and moths) that account for the majority of animal life on Earth. Diptera includes species known for their ubiquity (Musca domestica house fly), their role as pests (Anopheles gambiae malaria mosquito), and their value as model organisms across the biological sciences (Drosophila melanogaster). A resolved phylogeny for flies provides a framework for genomic, developmental, and evolutionary studies by facilitating comparisons across model organisms, yet recent research has suggested that fly relationships have been obscured by multiple episodes of rapid diversification. We provide a phylogenomic estimate of fly relationships based on molecules and morphology from 149 of 157 families, including 30 kb from 14 nuclear loci and complete mitochondrial genomes combined with 371 morphological characters. Multiple analyses show support for traditional groups (Brachycera, Cyclorrhapha, and Schizophora) and corroborate contentious findings, such as the anomalous Deuterophlebiidae as the sister group to all remaining Diptera. Our findings reveal that the closest relatives of the Drosophilidae are highly modified parasites (including the wingless Braulidae) of bees and other insects. Furthermore, we use micro-RNAs to resolve a node with implications for the evolution of embryonic development in Diptera. We demonstrate that flies experienced three episodes of rapid radiation—lower Diptera (220 Ma), lower Brachycera (180 Ma), and Schizophora (65 Ma)—and a number of life history transitions to hematophagy, phytophagy, and parasitism in the history of fly evolution over 260 million y.",

author = "Wiegmann, {Brian M.} and Trautwein, {Michelle D.} and Winkler, {Isaac S.} and Barr, {Norman B.} and Jung-Wook Kim and Christine Lambkin and Bertone, {Matthew A.} and Cassel, {Brian K.} and Bayless, {Keith M.} and Heimberg, {Alysha M.} and Wheeler, {Benjamin M.} and Peterson, {Kevin J.} and Thomas Pape and Sinclair, {Bradley J.} and Skevington, {Jeffrey H.} and Vladimir Blagoderov and Jason Caravas and Kutty, {Sujatha Narayanan} and Urs Schmidt-Ott and Kampmeier, {Gail E.} and Thompson, {F. Christian} and Grimaldi, {David A.} and Beckenbach, {Andrew T.} and Courtney, {Gregory W.} and Markus Friedrich and Rudolf Meier and Yeates, {David K.}",

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T1 - Episodic radiations in the fly tree of life

AU - Wiegmann, Brian M.

AU - Trautwein, Michelle D.

AU - Winkler, Isaac S.

AU - Barr, Norman B.

AU - Kim, Jung-Wook

AU - Lambkin, Christine

AU - Bertone, Matthew A.

AU - Cassel, Brian K.

AU - Bayless, Keith M.

AU - Heimberg, Alysha M.

AU - Wheeler, Benjamin M.

AU - Peterson, Kevin J.

AU - Pape, Thomas

AU - Sinclair, Bradley J.

AU - Skevington, Jeffrey H.

AU - Blagoderov, Vladimir

AU - Caravas, Jason

AU - Kutty, Sujatha Narayanan

AU - Schmidt-Ott, Urs

AU - Kampmeier, Gail E.

AU - Thompson, F. Christian

AU - Grimaldi, David A.

AU - Beckenbach, Andrew T.

AU - Courtney, Gregory W.

AU - Friedrich, Markus

AU - Meier, Rudolf

AU - Yeates, David K.

PY - 2011/4/5

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N2 - Flies are one of four superradiations of insects (along with beetles, wasps, and moths) that account for the majority of animal life on Earth. Diptera includes species known for their ubiquity (Musca domestica house fly), their role as pests (Anopheles gambiae malaria mosquito), and their value as model organisms across the biological sciences (Drosophila melanogaster). A resolved phylogeny for flies provides a framework for genomic, developmental, and evolutionary studies by facilitating comparisons across model organisms, yet recent research has suggested that fly relationships have been obscured by multiple episodes of rapid diversification. We provide a phylogenomic estimate of fly relationships based on molecules and morphology from 149 of 157 families, including 30 kb from 14 nuclear loci and complete mitochondrial genomes combined with 371 morphological characters. Multiple analyses show support for traditional groups (Brachycera, Cyclorrhapha, and Schizophora) and corroborate contentious findings, such as the anomalous Deuterophlebiidae as the sister group to all remaining Diptera. Our findings reveal that the closest relatives of the Drosophilidae are highly modified parasites (including the wingless Braulidae) of bees and other insects. Furthermore, we use micro-RNAs to resolve a node with implications for the evolution of embryonic development in Diptera. We demonstrate that flies experienced three episodes of rapid radiation—lower Diptera (220 Ma), lower Brachycera (180 Ma), and Schizophora (65 Ma)—and a number of life history transitions to hematophagy, phytophagy, and parasitism in the history of fly evolution over 260 million y.

AB - Flies are one of four superradiations of insects (along with beetles, wasps, and moths) that account for the majority of animal life on Earth. Diptera includes species known for their ubiquity (Musca domestica house fly), their role as pests (Anopheles gambiae malaria mosquito), and their value as model organisms across the biological sciences (Drosophila melanogaster). A resolved phylogeny for flies provides a framework for genomic, developmental, and evolutionary studies by facilitating comparisons across model organisms, yet recent research has suggested that fly relationships have been obscured by multiple episodes of rapid diversification. We provide a phylogenomic estimate of fly relationships based on molecules and morphology from 149 of 157 families, including 30 kb from 14 nuclear loci and complete mitochondrial genomes combined with 371 morphological characters. Multiple analyses show support for traditional groups (Brachycera, Cyclorrhapha, and Schizophora) and corroborate contentious findings, such as the anomalous Deuterophlebiidae as the sister group to all remaining Diptera. Our findings reveal that the closest relatives of the Drosophilidae are highly modified parasites (including the wingless Braulidae) of bees and other insects. Furthermore, we use micro-RNAs to resolve a node with implications for the evolution of embryonic development in Diptera. We demonstrate that flies experienced three episodes of rapid radiation—lower Diptera (220 Ma), lower Brachycera (180 Ma), and Schizophora (65 Ma)—and a number of life history transitions to hematophagy, phytophagy, and parasitism in the history of fly evolution over 260 million y.

U2 - 10.1073/pnas.1012675108

DO - 10.1073/pnas.1012675108

M3 - Journal article

SN - 0027-8424

VL - 108

SP - 5690

EP - 5695

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 14

ER -

Episodic radiations in the fly tree of life

Abstract

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