Global diversification of anelosimus spiders driven by long-distance overwater dispersal and neogene climate oscillations

Yufa Luo; Seok P. Goh; Daiqin Li; Marcelo O. Gonzaga; Adalberto J. Santos; Akio Tanikawa; Hajime Yoshida; Charles R. Haddad; Laura J. May-Collado; Matjaž Gregorič; Eva Turk; Matjaž Kuntner; Ingi Agnarsson

doi:10.1093/sysbio/syaa017

Global diversification of anelosimus spiders driven by long-distance overwater dispersal and neogene climate oscillations

Yufa Luo, Seok P. Goh, Daiqin Li, Marcelo O. Gonzaga, Adalberto J. Santos, Akio Tanikawa, Hajime Yoshida, Charles R. Haddad, Laura J. May-Collado, Matjaž Gregorič, Eva Turk, Matjaž Kuntner, Ingi Agnarsson^*

^*Corresponding author for this work

Faculty of Life and Environmental Sciences

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

8 Citations (Scopus)

Abstract

Vicariance and dispersal events, combined with intricate global climatic history, have left an imprint on the spatiotemporal distribution and diversity of many organisms. Anelosimus cobweb spiders (Theridiidae), are organisms ranging in behavior from solitary to highly social, with a cosmopolitan distribution in temperate to tropical areas. Their evolutionary history and the discontinuous distribution of species richness suggest that 1) long-distance overwater dispersal and 2) climate change during the Neogene (23-2.6 Ma), may be major factors in explaining their distribution and diversification. Here, we test these hypotheses, and explicitly test if global Miocene/Pliocene climatic cooling in the last 8 Ma affected Anelosimus radiation in parallel in South America and Madagascar. To do so, we investigate the phylogeny and spatiotemporal biogeography of Anelosimus through a culmination of a 20-year comprehensive global sampling at the species level (69 species, including 84% of the known 75 species worldwide, represented by 268 individuals) using nucleotide data from seven loci (5.5 kb). Our results strongly support the monophyly of Anelosimus with an Oligocene (∼30 Ma) South American origin. Major clades on other continents originate via multiple, long-distance dispersal events, of solitary or subsocial-but not social-lineages, from the Americas. These intercontinental dispersals were to Africa, Madagascar (twice), and SE Asia/Australasia. The early diversification of Anelosimus spiders coincides with a sudden thermal increase in the late Oligocene (∼27-25 Ma), though no causal connection can be made. Our results, however, strongly support the hypothesis that global Neogene climatic cooling in the last 8 Ma drove Anelosimus radiation in parallel in South America and Madagascar, offering a rare empirical evidence for diversification of a socially diverse group driven by an interplay between long-distance dispersal and global Neogene climatic changes.

Original language	English
Pages (from-to)	1122-1136
Number of pages	15
Journal	Systematic Biology
Volume	69
Issue number	6
DOIs	https://doi.org/10.1093/sysbio/syaa017
Publication status	Published - 1 Nov 2020

Bibliographical note

Funding Information:
This research was funded by a Slovenian Research Agency ARRS grant (ARRS Z1-9799-0618-07) and, in part, from National Geographic Society, UVM and NSF DEB-349205-1050187-1050253 to I.A. and G. Binford. Additional support came from National Geographic Society (8655-09, GEFNE29-11) to I.A., Killam Postdoctoral Fellowship to I.A., Fulbright support for foreign students (IIE 159 85610) to I.A., and the Sallee Charitable Trust to I.A. and M.K., the National Natural Science Foundation of China (NSFC)-31860602 grants 31660611 and 31460554, Natural Science Foundation of Jiangxi (20192BAB204008), and the Key Project of Science and Technology of Jiangxi (20161BBF60076) to Y.L.; Fundação de Amparo á Pesquisa do Estado de Minas Gerais (PPM-00605-17), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (407288/2013-9, 306222/2015-9, 405795/2016-5), and Instituto Nacional de Ciência e Tecnologia dos Hymenoptera Parasitóides da Região Sudeste Brasileira (Hympar/Sudeste, http://www.hympar.ufscar.br/, CNPq 465562/2014-0, FAPESP 2014/50940-2) to A.J.S.; Singapore Ministry of Education AcRF grants (R-154-000-435-112 and R-154-000-A52-114) to D.L.; and CNPq (311823/2017-3) to M.O.G. I.A. thanks Leticia Aviles and Wayne Maddison for long-term collaboration on projects leading to this work. Field and laboratory assistance came from too large a number of people, over the last 20 years, to fully detail here. Special thanks to Patricio Salazar and Gabriel Ituralde for collaboration with fieldwork in South America and Sahondra Hanitriniaina and Honoré Rabarison for assistance with field collections in Madagascar. We are grateful to Patricia Wright, Fredrica van Berkum, Benjamin Andriamihaja and all the ANGAP/MICET/MNP crew in Antananarivo and Périnet for logistical help during fieldwork in Madagascar. Yadira Ortiz Ruiz and Carol Yablonsky assisted with the molecular work of part of this study. Joerg Wunderlich provided specimens for DNA analyses. All material was collected under appropriate collection permits and approved guidelines

Publisher Copyright:
© The Author(s) 2020. Published by Oxford University Press, on behalf of the Society of Systematic Biologists. All rights reserved. For permissions, please email: [email protected]

Other keywords

Cobweb spiders
Diversification
Global biogeography
Long-distance dispersal
Molecular phylogenetics
Neogene climate changes
Sociality
Vicariance

Access to Document

10.1093/sysbio/syaa017

Cite this

Luo, Y., Goh, S. P., Li, D., Gonzaga, M. O., Santos, A. J., Tanikawa, A., Yoshida, H., Haddad, C. R., May-Collado, L. J., Gregorič, M., Turk, E., Kuntner, M., & Agnarsson, I. (2020). Global diversification of anelosimus spiders driven by long-distance overwater dispersal and neogene climate oscillations. Systematic Biology, 69(6), 1122-1136. https://doi.org/10.1093/sysbio/syaa017

@article{133c83283f974f1787f9b6564f44ac25,

title = "Global diversification of anelosimus spiders driven by long-distance overwater dispersal and neogene climate oscillations",

abstract = "Vicariance and dispersal events, combined with intricate global climatic history, have left an imprint on the spatiotemporal distribution and diversity of many organisms. Anelosimus cobweb spiders (Theridiidae), are organisms ranging in behavior from solitary to highly social, with a cosmopolitan distribution in temperate to tropical areas. Their evolutionary history and the discontinuous distribution of species richness suggest that 1) long-distance overwater dispersal and 2) climate change during the Neogene (23-2.6 Ma), may be major factors in explaining their distribution and diversification. Here, we test these hypotheses, and explicitly test if global Miocene/Pliocene climatic cooling in the last 8 Ma affected Anelosimus radiation in parallel in South America and Madagascar. To do so, we investigate the phylogeny and spatiotemporal biogeography of Anelosimus through a culmination of a 20-year comprehensive global sampling at the species level (69 species, including 84% of the known 75 species worldwide, represented by 268 individuals) using nucleotide data from seven loci (5.5 kb). Our results strongly support the monophyly of Anelosimus with an Oligocene (∼30 Ma) South American origin. Major clades on other continents originate via multiple, long-distance dispersal events, of solitary or subsocial-but not social-lineages, from the Americas. These intercontinental dispersals were to Africa, Madagascar (twice), and SE Asia/Australasia. The early diversification of Anelosimus spiders coincides with a sudden thermal increase in the late Oligocene (∼27-25 Ma), though no causal connection can be made. Our results, however, strongly support the hypothesis that global Neogene climatic cooling in the last 8 Ma drove Anelosimus radiation in parallel in South America and Madagascar, offering a rare empirical evidence for diversification of a socially diverse group driven by an interplay between long-distance dispersal and global Neogene climatic changes.",

keywords = "Cobweb spiders, Diversification, Global biogeography, Long-distance dispersal, Molecular phylogenetics, Neogene climate changes, Sociality, Vicariance",

author = "Yufa Luo and Goh, {Seok P.} and Daiqin Li and Gonzaga, {Marcelo O.} and Santos, {Adalberto J.} and Akio Tanikawa and Hajime Yoshida and Haddad, {Charles R.} and May-Collado, {Laura J.} and Matja{\v z} Gregori{\v c} and Eva Turk and Matja{\v z} Kuntner and Ingi Agnarsson",

note = "Funding Information: This research was funded by a Slovenian Research Agency ARRS grant (ARRS Z1-9799-0618-07) and, in part, from National Geographic Society, UVM and NSF DEB-349205-1050187-1050253 to I.A. and G. Binford. Additional support came from National Geographic Society (8655-09, GEFNE29-11) to I.A., Killam Postdoctoral Fellowship to I.A., Fulbright support for foreign students (IIE 159 85610) to I.A., and the Sallee Charitable Trust to I.A. and M.K., the National Natural Science Foundation of China (NSFC)-31860602 grants 31660611 and 31460554, Natural Science Foundation of Jiangxi (20192BAB204008), and the Key Project of Science and Technology of Jiangxi (20161BBF60076) to Y.L.; Funda{\c c}{\~a}o de Amparo {\'a} Pesquisa do Estado de Minas Gerais (PPM-00605-17), Conselho Nacional de Desenvolvimento Cient{\'i}fico e Tecnol{\'o}gico (CNPq) (407288/2013-9, 306222/2015-9, 405795/2016-5), and Instituto Nacional de Ci{\^e}ncia e Tecnologia dos Hymenoptera Parasit{\'o}ides da Regi{\~a}o Sudeste Brasileira (Hympar/Sudeste, http://www.hympar.ufscar.br/, CNPq 465562/2014-0, FAPESP 2014/50940-2) to A.J.S.; Singapore Ministry of Education AcRF grants (R-154-000-435-112 and R-154-000-A52-114) to D.L.; and CNPq (311823/2017-3) to M.O.G. I.A. thanks Leticia Aviles and Wayne Maddison for long-term collaboration on projects leading to this work. Field and laboratory assistance came from too large a number of people, over the last 20 years, to fully detail here. Special thanks to Patricio Salazar and Gabriel Ituralde for collaboration with fieldwork in South America and Sahondra Hanitriniaina and Honor{\'e} Rabarison for assistance with field collections in Madagascar. We are grateful to Patricia Wright, Fredrica van Berkum, Benjamin Andriamihaja and all the ANGAP/MICET/MNP crew in Antananarivo and P{\'e}rinet for logistical help during fieldwork in Madagascar. Yadira Ortiz Ruiz and Carol Yablonsky assisted with the molecular work of part of this study. Joerg Wunderlich provided specimens for DNA analyses. All material was collected under appropriate collection permits and approved guidelines Publisher Copyright: {\textcopyright} The Author(s) 2020. Published by Oxford University Press, on behalf of the Society of Systematic Biologists. All rights reserved. For permissions, please email: [email protected]",

year = "2020",

month = nov,

day = "1",

doi = "10.1093/sysbio/syaa017",

language = "English",

volume = "69",

pages = "1122--1136",

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Luo, Y, Goh, SP, Li, D, Gonzaga, MO, Santos, AJ, Tanikawa, A, Yoshida, H, Haddad, CR, May-Collado, LJ, Gregorič, M, Turk, E, Kuntner, M & Agnarsson, I 2020, 'Global diversification of anelosimus spiders driven by long-distance overwater dispersal and neogene climate oscillations', Systematic Biology, vol. 69, no. 6, pp. 1122-1136. https://doi.org/10.1093/sysbio/syaa017

TY - JOUR

T1 - Global diversification of anelosimus spiders driven by long-distance overwater dispersal and neogene climate oscillations

AU - Luo, Yufa

AU - Goh, Seok P.

AU - Li, Daiqin

AU - Gonzaga, Marcelo O.

AU - Santos, Adalberto J.

AU - Tanikawa, Akio

AU - Yoshida, Hajime

AU - Haddad, Charles R.

AU - May-Collado, Laura J.

AU - Gregorič, Matjaž

AU - Turk, Eva

AU - Kuntner, Matjaž

AU - Agnarsson, Ingi

N1 - Funding Information: This research was funded by a Slovenian Research Agency ARRS grant (ARRS Z1-9799-0618-07) and, in part, from National Geographic Society, UVM and NSF DEB-349205-1050187-1050253 to I.A. and G. Binford. Additional support came from National Geographic Society (8655-09, GEFNE29-11) to I.A., Killam Postdoctoral Fellowship to I.A., Fulbright support for foreign students (IIE 159 85610) to I.A., and the Sallee Charitable Trust to I.A. and M.K., the National Natural Science Foundation of China (NSFC)-31860602 grants 31660611 and 31460554, Natural Science Foundation of Jiangxi (20192BAB204008), and the Key Project of Science and Technology of Jiangxi (20161BBF60076) to Y.L.; Fundação de Amparo á Pesquisa do Estado de Minas Gerais (PPM-00605-17), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (407288/2013-9, 306222/2015-9, 405795/2016-5), and Instituto Nacional de Ciência e Tecnologia dos Hymenoptera Parasitóides da Região Sudeste Brasileira (Hympar/Sudeste, http://www.hympar.ufscar.br/, CNPq 465562/2014-0, FAPESP 2014/50940-2) to A.J.S.; Singapore Ministry of Education AcRF grants (R-154-000-435-112 and R-154-000-A52-114) to D.L.; and CNPq (311823/2017-3) to M.O.G. I.A. thanks Leticia Aviles and Wayne Maddison for long-term collaboration on projects leading to this work. Field and laboratory assistance came from too large a number of people, over the last 20 years, to fully detail here. Special thanks to Patricio Salazar and Gabriel Ituralde for collaboration with fieldwork in South America and Sahondra Hanitriniaina and Honoré Rabarison for assistance with field collections in Madagascar. We are grateful to Patricia Wright, Fredrica van Berkum, Benjamin Andriamihaja and all the ANGAP/MICET/MNP crew in Antananarivo and Périnet for logistical help during fieldwork in Madagascar. Yadira Ortiz Ruiz and Carol Yablonsky assisted with the molecular work of part of this study. Joerg Wunderlich provided specimens for DNA analyses. All material was collected under appropriate collection permits and approved guidelines Publisher Copyright: © The Author(s) 2020. Published by Oxford University Press, on behalf of the Society of Systematic Biologists. All rights reserved. For permissions, please email: [email protected]

PY - 2020/11/1

Y1 - 2020/11/1

N2 - Vicariance and dispersal events, combined with intricate global climatic history, have left an imprint on the spatiotemporal distribution and diversity of many organisms. Anelosimus cobweb spiders (Theridiidae), are organisms ranging in behavior from solitary to highly social, with a cosmopolitan distribution in temperate to tropical areas. Their evolutionary history and the discontinuous distribution of species richness suggest that 1) long-distance overwater dispersal and 2) climate change during the Neogene (23-2.6 Ma), may be major factors in explaining their distribution and diversification. Here, we test these hypotheses, and explicitly test if global Miocene/Pliocene climatic cooling in the last 8 Ma affected Anelosimus radiation in parallel in South America and Madagascar. To do so, we investigate the phylogeny and spatiotemporal biogeography of Anelosimus through a culmination of a 20-year comprehensive global sampling at the species level (69 species, including 84% of the known 75 species worldwide, represented by 268 individuals) using nucleotide data from seven loci (5.5 kb). Our results strongly support the monophyly of Anelosimus with an Oligocene (∼30 Ma) South American origin. Major clades on other continents originate via multiple, long-distance dispersal events, of solitary or subsocial-but not social-lineages, from the Americas. These intercontinental dispersals were to Africa, Madagascar (twice), and SE Asia/Australasia. The early diversification of Anelosimus spiders coincides with a sudden thermal increase in the late Oligocene (∼27-25 Ma), though no causal connection can be made. Our results, however, strongly support the hypothesis that global Neogene climatic cooling in the last 8 Ma drove Anelosimus radiation in parallel in South America and Madagascar, offering a rare empirical evidence for diversification of a socially diverse group driven by an interplay between long-distance dispersal and global Neogene climatic changes.

AB - Vicariance and dispersal events, combined with intricate global climatic history, have left an imprint on the spatiotemporal distribution and diversity of many organisms. Anelosimus cobweb spiders (Theridiidae), are organisms ranging in behavior from solitary to highly social, with a cosmopolitan distribution in temperate to tropical areas. Their evolutionary history and the discontinuous distribution of species richness suggest that 1) long-distance overwater dispersal and 2) climate change during the Neogene (23-2.6 Ma), may be major factors in explaining their distribution and diversification. Here, we test these hypotheses, and explicitly test if global Miocene/Pliocene climatic cooling in the last 8 Ma affected Anelosimus radiation in parallel in South America and Madagascar. To do so, we investigate the phylogeny and spatiotemporal biogeography of Anelosimus through a culmination of a 20-year comprehensive global sampling at the species level (69 species, including 84% of the known 75 species worldwide, represented by 268 individuals) using nucleotide data from seven loci (5.5 kb). Our results strongly support the monophyly of Anelosimus with an Oligocene (∼30 Ma) South American origin. Major clades on other continents originate via multiple, long-distance dispersal events, of solitary or subsocial-but not social-lineages, from the Americas. These intercontinental dispersals were to Africa, Madagascar (twice), and SE Asia/Australasia. The early diversification of Anelosimus spiders coincides with a sudden thermal increase in the late Oligocene (∼27-25 Ma), though no causal connection can be made. Our results, however, strongly support the hypothesis that global Neogene climatic cooling in the last 8 Ma drove Anelosimus radiation in parallel in South America and Madagascar, offering a rare empirical evidence for diversification of a socially diverse group driven by an interplay between long-distance dispersal and global Neogene climatic changes.

KW - Cobweb spiders

KW - Diversification

KW - Global biogeography

KW - Long-distance dispersal

KW - Molecular phylogenetics

KW - Neogene climate changes

KW - Sociality

KW - Vicariance

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U2 - 10.1093/sysbio/syaa017

DO - 10.1093/sysbio/syaa017

M3 - Article

C2 - 32170955

AN - SCOPUS:85091382660

SN - 1063-5157

VL - 69

SP - 1122

EP - 1136

JO - Systematic Biology

JF - Systematic Biology

IS - 6

ER -

Global diversification of anelosimus spiders driven by long-distance overwater dispersal and neogene climate oscillations

Abstract

Bibliographical note

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