Neglected no longer: Phylogenomic resolution of higher-level relationships in Solifugae

Siddharth S. Kulkarni; Hugh G. Steiner; Erika L. Garcia; Hernán Iuri; R. Ryan Jones; Jesús A. Ballesteros; Guilherme Gainett; Matthew R. Graham; Danilo Harms; Robin Lyle; Andrés A. Ojanguren-Affilastro; Carlos E. Santibañez-López; Gustavo Silva de Miranda; Paula E. Cushing; Efrat Gavish-Regev; Prashant P. Sharma

doi:10.1016/j.isci.2023.107684

Neglected no longer: Phylogenomic resolution of higher-level relationships in Solifugae

Siddharth S. Kulkarni^*, Hugh G. Steiner, Erika L. Garcia, Hernán Iuri, R. Ryan Jones, Jesús A. Ballesteros, Guilherme Gainett, Matthew R. Graham, Danilo Harms, Robin Lyle, Andrés A. Ojanguren-Affilastro, Carlos E. Santibañez-López, Gustavo Silva de Miranda, Paula E. Cushing, Efrat Gavish-Regev, Prashant P. Sharma

^*Corresponding author for this work

National Natural History Collections

Research output: Contribution to journal › Article › peer-review

Abstract

Advanced sequencing technologies have expedited resolution of higher-level arthropod relationships. Yet, dark branches persist, principally among groups occurring in cryptic habitats. Among chelicerates, Solifugae (“camel spiders”) is the last order lacking a higher-level phylogeny and have thus been historically characterized as “neglected [arachnid] cousins”. Though renowned for aggression, remarkable running speed, and xeric adaptation, inferring solifuge relationships has been hindered by inaccessibility of diagnostic morphological characters, whereas molecular investigations have been limited to one of 12 recognized families. Our phylogenomic dataset via capture of ultraconserved elements sampling all extant families recovered a well-resolved phylogeny, with two distinct groups of New World taxa nested within a broader Paleotropical radiation. Divergence times using fossil calibrations inferred that Solifugae radiated by the Permian, and most families diverged prior to the Paleogene-Cretaceous extinction, likely driven by continental breakup. We establish Boreosolifugae new suborder uniting five Laurasian families, and Australosolifugae new suborder uniting seven Gondwanan families using morphological and biogeographic signal.

Original language	American English
Article number	107684
Journal	iScience
Volume	26
Issue number	9
DOIs	https://doi.org/10.1016/j.isci.2023.107684
State	Published - 15 Sep 2023

Bibliographical note

Funding Information:
We are grateful to Nuria Macias (Departamento de Zoología de la Universidad de La Laguna) for providing a specimen of Eusimonia wunderlichi from the Canary Islands, and to Marc Domènech and Miquel Arnedo (University of Barcelona) for providing a specimen of Gluvia dorsalis from Spain. Photographs of live specimens were kindly provided by Igor Armiach Steinpress and Shlomi Aharon. Sequencing was performed at the Biotechnology Center of the University of Wisconsin-Madison. We thank Gustavo Hormiga for access to the Colonial One High Performance Computing Facility at The George Washington University to conduct some of the analyses. This project was supported by Binational Science Foundation grant no. BSF-2019216 to E.G.R. and P.P.S.; and National Science Foundation grant no. DEB-1754587 to P.E.C. S.S.K. G.G. and P.P.S. were additionally supported by National Science Foundation NSF grant no. IOS-2016141 to P.P.S. Conceptualization, S.K. P.E.C. A.A.O.A. E.G.R. and P.S.; Methodology, S.K. H.S. H.I. and P.S.; Resources, E.L.G. H.I. R.J. J.A.B. G.G. M.R.G. D.H. R.L. A.A.O.A. C.E.S.L. G.S.D.M. P.E.C. E.G.R. and P.S. Writing – Original Draft, S.K. and P.S.; Writing – Review and Editing, H.S. E.L.G. H.I. R.J. J.A.B. G.G. M.R.G. D.H. R.L. A.A.O.A. C.E.S.L. G.S.D.M. P.E.C. E.G.R. and P.S. Supervision, P.S.; Project Administration, P.S.; Funding Acquisition, E.G.R. and P.S. The authors declare no competing interests. We support inclusive, diverse, and equitable conduct of research.

Funding Information:
We are grateful to Nuria Macias (Departamento de Zoología de la Universidad de La Laguna) for providing a specimen of Eusimonia wunderlichi from the Canary Islands, and to Marc Domènech and Miquel Arnedo (University of Barcelona) for providing a specimen of Gluvia dorsalis from Spain. Photographs of live specimens were kindly provided by Igor Armiach Steinpress and Shlomi Aharon. Sequencing was performed at the Biotechnology Center of the University of Wisconsin-Madison. We thank Gustavo Hormiga for access to the Colonial One High Performance Computing Facility at The George Washington University to conduct some of the analyses. This project was supported by Binational Science Foundation grant no. BSF-2019216 to E.G.R. and P.P.S.; and National Science Foundation grant no. DEB-1754587 to P.E.C. S.S.K., G.G., and P.P.S. were additionally supported by National Science Foundation NSF grant no. IOS-2016141 to P.P.S.

Publisher Copyright:
© 2023 The Author(s)

Keywords

Evolutionary biology
Phylogenetics
Phylogeny
Zoology

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10.1016/j.isci.2023.107684

Cite this

Kulkarni, S. S., Steiner, H. G., Garcia, E. L., Iuri, H., Jones, R. R., Ballesteros, J. A., Gainett, G., Graham, M. R., Harms, D., Lyle, R., Ojanguren-Affilastro, A. A., Santibañez-López, C. E., Silva de Miranda, G., Cushing, P. E., Gavish-Regev, E., & Sharma, P. P. (2023). Neglected no longer: Phylogenomic resolution of higher-level relationships in Solifugae. iScience, 26(9), Article 107684. https://doi.org/10.1016/j.isci.2023.107684

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title = "Neglected no longer: Phylogenomic resolution of higher-level relationships in Solifugae",

abstract = "Advanced sequencing technologies have expedited resolution of higher-level arthropod relationships. Yet, dark branches persist, principally among groups occurring in cryptic habitats. Among chelicerates, Solifugae (“camel spiders”) is the last order lacking a higher-level phylogeny and have thus been historically characterized as “neglected [arachnid] cousins”. Though renowned for aggression, remarkable running speed, and xeric adaptation, inferring solifuge relationships has been hindered by inaccessibility of diagnostic morphological characters, whereas molecular investigations have been limited to one of 12 recognized families. Our phylogenomic dataset via capture of ultraconserved elements sampling all extant families recovered a well-resolved phylogeny, with two distinct groups of New World taxa nested within a broader Paleotropical radiation. Divergence times using fossil calibrations inferred that Solifugae radiated by the Permian, and most families diverged prior to the Paleogene-Cretaceous extinction, likely driven by continental breakup. We establish Boreosolifugae new suborder uniting five Laurasian families, and Australosolifugae new suborder uniting seven Gondwanan families using morphological and biogeographic signal.",

keywords = "Evolutionary biology, Phylogenetics, Phylogeny, Zoology",

author = "Kulkarni, {Siddharth S.} and Steiner, {Hugh G.} and Garcia, {Erika L.} and Hern{\'a}n Iuri and Jones, {R. Ryan} and Ballesteros, {Jes{\'u}s A.} and Guilherme Gainett and Graham, {Matthew R.} and Danilo Harms and Robin Lyle and Ojanguren-Affilastro, {Andr{\'e}s A.} and Santiba{\~n}ez-L{\'o}pez, {Carlos E.} and {Silva de Miranda}, Gustavo and Cushing, {Paula E.} and Efrat Gavish-Regev and Sharma, {Prashant P.}",

note = "Funding Information: We are grateful to Nuria Macias (Departamento de Zoolog{\'i}a de la Universidad de La Laguna) for providing a specimen of Eusimonia wunderlichi from the Canary Islands, and to Marc Dom{\`e}nech and Miquel Arnedo (University of Barcelona) for providing a specimen of Gluvia dorsalis from Spain. Photographs of live specimens were kindly provided by Igor Armiach Steinpress and Shlomi Aharon. Sequencing was performed at the Biotechnology Center of the University of Wisconsin-Madison. We thank Gustavo Hormiga for access to the Colonial One High Performance Computing Facility at The George Washington University to conduct some of the analyses. This project was supported by Binational Science Foundation grant no. BSF-2019216 to E.G.R. and P.P.S.; and National Science Foundation grant no. DEB-1754587 to P.E.C. S.S.K. G.G. and P.P.S. were additionally supported by National Science Foundation NSF grant no. IOS-2016141 to P.P.S. Conceptualization, S.K. P.E.C. A.A.O.A. E.G.R. and P.S.; Methodology, S.K. H.S. H.I. and P.S.; Resources, E.L.G. H.I. R.J. J.A.B. G.G. M.R.G. D.H. R.L. A.A.O.A. C.E.S.L. G.S.D.M. P.E.C. E.G.R. and P.S. Writing – Original Draft, S.K. and P.S.; Writing – Review and Editing, H.S. E.L.G. H.I. R.J. J.A.B. G.G. M.R.G. D.H. R.L. A.A.O.A. C.E.S.L. G.S.D.M. P.E.C. E.G.R. and P.S. Supervision, P.S.; Project Administration, P.S.; Funding Acquisition, E.G.R. and P.S. The authors declare no competing interests. We support inclusive, diverse, and equitable conduct of research. Funding Information: We are grateful to Nuria Macias (Departamento de Zoolog{\'i}a de la Universidad de La Laguna) for providing a specimen of Eusimonia wunderlichi from the Canary Islands, and to Marc Dom{\`e}nech and Miquel Arnedo (University of Barcelona) for providing a specimen of Gluvia dorsalis from Spain. Photographs of live specimens were kindly provided by Igor Armiach Steinpress and Shlomi Aharon. Sequencing was performed at the Biotechnology Center of the University of Wisconsin-Madison. We thank Gustavo Hormiga for access to the Colonial One High Performance Computing Facility at The George Washington University to conduct some of the analyses. This project was supported by Binational Science Foundation grant no. BSF-2019216 to E.G.R. and P.P.S.; and National Science Foundation grant no. DEB-1754587 to P.E.C. S.S.K., G.G., and P.P.S. were additionally supported by National Science Foundation NSF grant no. IOS-2016141 to P.P.S. Publisher Copyright: {\textcopyright} 2023 The Author(s)",

year = "2023",

month = sep,

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doi = "10.1016/j.isci.2023.107684",

language = "American English",

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Kulkarni, SS, Steiner, HG, Garcia, EL, Iuri, H, Jones, RR, Ballesteros, JA, Gainett, G, Graham, MR, Harms, D, Lyle, R, Ojanguren-Affilastro, AA, Santibañez-López, CE, Silva de Miranda, G, Cushing, PE, Gavish-Regev, E & Sharma, PP 2023, 'Neglected no longer: Phylogenomic resolution of higher-level relationships in Solifugae', iScience, vol. 26, no. 9, 107684. https://doi.org/10.1016/j.isci.2023.107684

TY - JOUR

T1 - Neglected no longer

T2 - Phylogenomic resolution of higher-level relationships in Solifugae

AU - Kulkarni, Siddharth S.

AU - Steiner, Hugh G.

AU - Garcia, Erika L.

AU - Iuri, Hernán

AU - Jones, R. Ryan

AU - Ballesteros, Jesús A.

AU - Gainett, Guilherme

AU - Graham, Matthew R.

AU - Harms, Danilo

AU - Lyle, Robin

AU - Ojanguren-Affilastro, Andrés A.

AU - Santibañez-López, Carlos E.

AU - Silva de Miranda, Gustavo

AU - Cushing, Paula E.

AU - Gavish-Regev, Efrat

AU - Sharma, Prashant P.

N1 - Funding Information: We are grateful to Nuria Macias (Departamento de Zoología de la Universidad de La Laguna) for providing a specimen of Eusimonia wunderlichi from the Canary Islands, and to Marc Domènech and Miquel Arnedo (University of Barcelona) for providing a specimen of Gluvia dorsalis from Spain. Photographs of live specimens were kindly provided by Igor Armiach Steinpress and Shlomi Aharon. Sequencing was performed at the Biotechnology Center of the University of Wisconsin-Madison. We thank Gustavo Hormiga for access to the Colonial One High Performance Computing Facility at The George Washington University to conduct some of the analyses. This project was supported by Binational Science Foundation grant no. BSF-2019216 to E.G.R. and P.P.S.; and National Science Foundation grant no. DEB-1754587 to P.E.C. S.S.K. G.G. and P.P.S. were additionally supported by National Science Foundation NSF grant no. IOS-2016141 to P.P.S. Conceptualization, S.K. P.E.C. A.A.O.A. E.G.R. and P.S.; Methodology, S.K. H.S. H.I. and P.S.; Resources, E.L.G. H.I. R.J. J.A.B. G.G. M.R.G. D.H. R.L. A.A.O.A. C.E.S.L. G.S.D.M. P.E.C. E.G.R. and P.S. Writing – Original Draft, S.K. and P.S.; Writing – Review and Editing, H.S. E.L.G. H.I. R.J. J.A.B. G.G. M.R.G. D.H. R.L. A.A.O.A. C.E.S.L. G.S.D.M. P.E.C. E.G.R. and P.S. Supervision, P.S.; Project Administration, P.S.; Funding Acquisition, E.G.R. and P.S. The authors declare no competing interests. We support inclusive, diverse, and equitable conduct of research. Funding Information: We are grateful to Nuria Macias (Departamento de Zoología de la Universidad de La Laguna) for providing a specimen of Eusimonia wunderlichi from the Canary Islands, and to Marc Domènech and Miquel Arnedo (University of Barcelona) for providing a specimen of Gluvia dorsalis from Spain. Photographs of live specimens were kindly provided by Igor Armiach Steinpress and Shlomi Aharon. Sequencing was performed at the Biotechnology Center of the University of Wisconsin-Madison. We thank Gustavo Hormiga for access to the Colonial One High Performance Computing Facility at The George Washington University to conduct some of the analyses. This project was supported by Binational Science Foundation grant no. BSF-2019216 to E.G.R. and P.P.S.; and National Science Foundation grant no. DEB-1754587 to P.E.C. S.S.K., G.G., and P.P.S. were additionally supported by National Science Foundation NSF grant no. IOS-2016141 to P.P.S. Publisher Copyright: © 2023 The Author(s)

PY - 2023/9/15

Y1 - 2023/9/15

N2 - Advanced sequencing technologies have expedited resolution of higher-level arthropod relationships. Yet, dark branches persist, principally among groups occurring in cryptic habitats. Among chelicerates, Solifugae (“camel spiders”) is the last order lacking a higher-level phylogeny and have thus been historically characterized as “neglected [arachnid] cousins”. Though renowned for aggression, remarkable running speed, and xeric adaptation, inferring solifuge relationships has been hindered by inaccessibility of diagnostic morphological characters, whereas molecular investigations have been limited to one of 12 recognized families. Our phylogenomic dataset via capture of ultraconserved elements sampling all extant families recovered a well-resolved phylogeny, with two distinct groups of New World taxa nested within a broader Paleotropical radiation. Divergence times using fossil calibrations inferred that Solifugae radiated by the Permian, and most families diverged prior to the Paleogene-Cretaceous extinction, likely driven by continental breakup. We establish Boreosolifugae new suborder uniting five Laurasian families, and Australosolifugae new suborder uniting seven Gondwanan families using morphological and biogeographic signal.

AB - Advanced sequencing technologies have expedited resolution of higher-level arthropod relationships. Yet, dark branches persist, principally among groups occurring in cryptic habitats. Among chelicerates, Solifugae (“camel spiders”) is the last order lacking a higher-level phylogeny and have thus been historically characterized as “neglected [arachnid] cousins”. Though renowned for aggression, remarkable running speed, and xeric adaptation, inferring solifuge relationships has been hindered by inaccessibility of diagnostic morphological characters, whereas molecular investigations have been limited to one of 12 recognized families. Our phylogenomic dataset via capture of ultraconserved elements sampling all extant families recovered a well-resolved phylogeny, with two distinct groups of New World taxa nested within a broader Paleotropical radiation. Divergence times using fossil calibrations inferred that Solifugae radiated by the Permian, and most families diverged prior to the Paleogene-Cretaceous extinction, likely driven by continental breakup. We establish Boreosolifugae new suborder uniting five Laurasian families, and Australosolifugae new suborder uniting seven Gondwanan families using morphological and biogeographic signal.

KW - Evolutionary biology

KW - Phylogenetics

KW - Phylogeny

KW - Zoology

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ER -

Neglected no longer: Phylogenomic resolution of higher-level relationships in Solifugae

Abstract

Bibliographical note

Keywords

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