Recent speciation and phenotypic plasticity within a parthenogenetic lineage of levantine whip spiders (Chelicerata: Amblypygi: Charinidae)

Caitlin M. Baker; Jesús A. Ballesteros; Shlomi Aharon; Guilherme Gainett; Igor Armiach Steinpress; Gil Wizen; Prashant P. Sharma; Efrat Gavish-Regev

doi:10.1016/j.ympev.2022.107560

Recent speciation and phenotypic plasticity within a parthenogenetic lineage of levantine whip spiders (Chelicerata: Amblypygi: Charinidae)

Caitlin M. Baker, Jesús A. Ballesteros, Shlomi Aharon, Guilherme Gainett, Igor Armiach Steinpress, Gil Wizen, Prashant P. Sharma, Efrat Gavish-Regev^*

^*Corresponding author for this work

National Natural History Collections

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

2 Scopus citations

Abstract

Caves constitute ideal study systems for investigating adaptation and speciation, as the abiotic conditions shared by aphotic habitats exert a set of environmental filters on their communities. Arachnids constitute an important component of many cave ecosystems worldwide. We investigated the population genomics of two whip spider species: Sarax ioanniticus, a widely distributed parthenogenetic species found across the eastern Mediterranean; and S. israelensis, a recently described troglomorphic species that is endemic to caves in Israel. Here, we show that S. israelensis is completely genetically distinct from S. ioanniticus and most likely also a parthenogen. Counterintuitively, despite the lack of genetic variability within S. ioanniticus and S. israelensis, we discovered considerable variation in the degree of median eye reduction, particularly in the latter species. Natural history data from captive-bred specimens of S. israelensis validated the interpretation of parthenogenesis. Our results are most consistent with a scenario of a sexual ancestral species that underwent speciation, followed by independent transitions to apomictic parthenogenesis in each of the two daughter species. Moreover, the lack of genetic variability suggests that variation in eye morphology in S. israelensis is driven exclusively by epigenetic mechanisms.

Original language	American English
Article number	107560
Journal	Molecular Phylogenetics and Evolution
Volume	175
DOIs	https://doi.org/10.1016/j.ympev.2022.107560
State	Published - Oct 2022

Bibliographical note

Funding Information:
We thank A. Frumkin, B. Langford, E. Cohen (Israel Cave Research Center), and E. Levin for assistance with cave data and in the field. Sequencing was performed at the UW-Madison Biotechnology Center. Access to computing was provided by the Bioinformatics Resource Center (BRC) of the University of Wisconsin-Madison. Fieldwork in Israel was supported by a National Geographic Society Expeditions Council grant no. NGS-271R-18 to J.A.B.. This work is supported by the US-Israel Binational Science Foundation grant no. BSF-2019216 to P.P.S. and E.G.-R. This manuscript was improved by valuable comments from the associate editor Mike Rix, and from Miquel Arnedo and one anonymous reviewer.

Funding Information:
Specimens of Amblypygi were collected under permits 2013/40027, 2013/40085, 2014/40313, 2017/41718 and 2020/42450, issued to E.G.-R.; and permits 2012/38653, 2013/40027, 2014/40313, 2014/40503 and 2016/41370, issued to G.W. by the Israel National Parks Authority. We thank A. Frumkin, B. Langford, E. Cohen (Israel Cave Research Center), and E. Levin for assistance with cave data and in the field. Sequencing was performed at the UW-Madison Biotechnology Center. Access to computing was provided by the Bioinformatics Resource Center (BRC) of the University of Wisconsin-Madison. Fieldwork in Israel was supported by a National Geographic Society Expeditions Council grant no. NGS-271R-18 to J.A.B. This work is supported by the US-Israel Binational Science Foundation grant no. BSF-2019216 to P.P.S. and E.G.-R. This manuscript was improved by valuable comments from the associate editor Mike Rix, and from Miquel Arnedo and one anonymous reviewer.

Publisher Copyright:
© 2022 Elsevier Inc.

Keywords

Genotyping-by-sequencing
Molecular clock
Population genomics
Sarax
Sympatry
Troglophile

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10.1016/j.ympev.2022.107560

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Baker, C. M., Ballesteros, J. A., Aharon, S., Gainett, G., Armiach Steinpress, I., Wizen, G., Sharma, P. P., & Gavish-Regev, E. (2022). Recent speciation and phenotypic plasticity within a parthenogenetic lineage of levantine whip spiders (Chelicerata: Amblypygi: Charinidae). Molecular Phylogenetics and Evolution, 175, Article 107560. https://doi.org/10.1016/j.ympev.2022.107560

@article{945b681f582d4ca8aae21b2a38e5e738,

title = "Recent speciation and phenotypic plasticity within a parthenogenetic lineage of levantine whip spiders (Chelicerata: Amblypygi: Charinidae)",

abstract = "Caves constitute ideal study systems for investigating adaptation and speciation, as the abiotic conditions shared by aphotic habitats exert a set of environmental filters on their communities. Arachnids constitute an important component of many cave ecosystems worldwide. We investigated the population genomics of two whip spider species: Sarax ioanniticus, a widely distributed parthenogenetic species found across the eastern Mediterranean; and S. israelensis, a recently described troglomorphic species that is endemic to caves in Israel. Here, we show that S. israelensis is completely genetically distinct from S. ioanniticus and most likely also a parthenogen. Counterintuitively, despite the lack of genetic variability within S. ioanniticus and S. israelensis, we discovered considerable variation in the degree of median eye reduction, particularly in the latter species. Natural history data from captive-bred specimens of S. israelensis validated the interpretation of parthenogenesis. Our results are most consistent with a scenario of a sexual ancestral species that underwent speciation, followed by independent transitions to apomictic parthenogenesis in each of the two daughter species. Moreover, the lack of genetic variability suggests that variation in eye morphology in S. israelensis is driven exclusively by epigenetic mechanisms.",

keywords = "Genotyping-by-sequencing, Molecular clock, Population genomics, Sarax, Sympatry, Troglophile",

author = "Baker, {Caitlin M.} and Ballesteros, {Jes{\'u}s A.} and Shlomi Aharon and Guilherme Gainett and {Armiach Steinpress}, Igor and Gil Wizen and Sharma, {Prashant P.} and Efrat Gavish-Regev",

note = "Funding Information: We thank A. Frumkin, B. Langford, E. Cohen (Israel Cave Research Center), and E. Levin for assistance with cave data and in the field. Sequencing was performed at the UW-Madison Biotechnology Center. Access to computing was provided by the Bioinformatics Resource Center (BRC) of the University of Wisconsin-Madison. Fieldwork in Israel was supported by a National Geographic Society Expeditions Council grant no. NGS-271R-18 to J.A.B.. This work is supported by the US-Israel Binational Science Foundation grant no. BSF-2019216 to P.P.S. and E.G.-R. This manuscript was improved by valuable comments from the associate editor Mike Rix, and from Miquel Arnedo and one anonymous reviewer. Funding Information: Specimens of Amblypygi were collected under permits 2013/40027, 2013/40085, 2014/40313, 2017/41718 and 2020/42450, issued to E.G.-R.; and permits 2012/38653, 2013/40027, 2014/40313, 2014/40503 and 2016/41370, issued to G.W. by the Israel National Parks Authority. We thank A. Frumkin, B. Langford, E. Cohen (Israel Cave Research Center), and E. Levin for assistance with cave data and in the field. Sequencing was performed at the UW-Madison Biotechnology Center. Access to computing was provided by the Bioinformatics Resource Center (BRC) of the University of Wisconsin-Madison. Fieldwork in Israel was supported by a National Geographic Society Expeditions Council grant no. NGS-271R-18 to J.A.B. This work is supported by the US-Israel Binational Science Foundation grant no. BSF-2019216 to P.P.S. and E.G.-R. This manuscript was improved by valuable comments from the associate editor Mike Rix, and from Miquel Arnedo and one anonymous reviewer. Publisher Copyright: {\textcopyright} 2022 Elsevier Inc.",

year = "2022",

month = oct,

doi = "10.1016/j.ympev.2022.107560",

language = "American English",

volume = "175",

journal = "Molecular Phylogenetics and Evolution",

issn = "1055-7903",

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T1 - Recent speciation and phenotypic plasticity within a parthenogenetic lineage of levantine whip spiders (Chelicerata: Amblypygi: Charinidae)

AU - Baker, Caitlin M.

AU - Ballesteros, Jesús A.

AU - Aharon, Shlomi

AU - Gainett, Guilherme

AU - Armiach Steinpress, Igor

AU - Wizen, Gil

AU - Sharma, Prashant P.

AU - Gavish-Regev, Efrat

N1 - Funding Information: We thank A. Frumkin, B. Langford, E. Cohen (Israel Cave Research Center), and E. Levin for assistance with cave data and in the field. Sequencing was performed at the UW-Madison Biotechnology Center. Access to computing was provided by the Bioinformatics Resource Center (BRC) of the University of Wisconsin-Madison. Fieldwork in Israel was supported by a National Geographic Society Expeditions Council grant no. NGS-271R-18 to J.A.B.. This work is supported by the US-Israel Binational Science Foundation grant no. BSF-2019216 to P.P.S. and E.G.-R. This manuscript was improved by valuable comments from the associate editor Mike Rix, and from Miquel Arnedo and one anonymous reviewer. Funding Information: Specimens of Amblypygi were collected under permits 2013/40027, 2013/40085, 2014/40313, 2017/41718 and 2020/42450, issued to E.G.-R.; and permits 2012/38653, 2013/40027, 2014/40313, 2014/40503 and 2016/41370, issued to G.W. by the Israel National Parks Authority. We thank A. Frumkin, B. Langford, E. Cohen (Israel Cave Research Center), and E. Levin for assistance with cave data and in the field. Sequencing was performed at the UW-Madison Biotechnology Center. Access to computing was provided by the Bioinformatics Resource Center (BRC) of the University of Wisconsin-Madison. Fieldwork in Israel was supported by a National Geographic Society Expeditions Council grant no. NGS-271R-18 to J.A.B. This work is supported by the US-Israel Binational Science Foundation grant no. BSF-2019216 to P.P.S. and E.G.-R. This manuscript was improved by valuable comments from the associate editor Mike Rix, and from Miquel Arnedo and one anonymous reviewer. Publisher Copyright: © 2022 Elsevier Inc.

PY - 2022/10

Y1 - 2022/10

N2 - Caves constitute ideal study systems for investigating adaptation and speciation, as the abiotic conditions shared by aphotic habitats exert a set of environmental filters on their communities. Arachnids constitute an important component of many cave ecosystems worldwide. We investigated the population genomics of two whip spider species: Sarax ioanniticus, a widely distributed parthenogenetic species found across the eastern Mediterranean; and S. israelensis, a recently described troglomorphic species that is endemic to caves in Israel. Here, we show that S. israelensis is completely genetically distinct from S. ioanniticus and most likely also a parthenogen. Counterintuitively, despite the lack of genetic variability within S. ioanniticus and S. israelensis, we discovered considerable variation in the degree of median eye reduction, particularly in the latter species. Natural history data from captive-bred specimens of S. israelensis validated the interpretation of parthenogenesis. Our results are most consistent with a scenario of a sexual ancestral species that underwent speciation, followed by independent transitions to apomictic parthenogenesis in each of the two daughter species. Moreover, the lack of genetic variability suggests that variation in eye morphology in S. israelensis is driven exclusively by epigenetic mechanisms.

AB - Caves constitute ideal study systems for investigating adaptation and speciation, as the abiotic conditions shared by aphotic habitats exert a set of environmental filters on their communities. Arachnids constitute an important component of many cave ecosystems worldwide. We investigated the population genomics of two whip spider species: Sarax ioanniticus, a widely distributed parthenogenetic species found across the eastern Mediterranean; and S. israelensis, a recently described troglomorphic species that is endemic to caves in Israel. Here, we show that S. israelensis is completely genetically distinct from S. ioanniticus and most likely also a parthenogen. Counterintuitively, despite the lack of genetic variability within S. ioanniticus and S. israelensis, we discovered considerable variation in the degree of median eye reduction, particularly in the latter species. Natural history data from captive-bred specimens of S. israelensis validated the interpretation of parthenogenesis. Our results are most consistent with a scenario of a sexual ancestral species that underwent speciation, followed by independent transitions to apomictic parthenogenesis in each of the two daughter species. Moreover, the lack of genetic variability suggests that variation in eye morphology in S. israelensis is driven exclusively by epigenetic mechanisms.

KW - Genotyping-by-sequencing

KW - Molecular clock

KW - Population genomics

KW - Sarax

KW - Sympatry

KW - Troglophile

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U2 - 10.1016/j.ympev.2022.107560

DO - 10.1016/j.ympev.2022.107560

M3 - Article

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AN - SCOPUS:85134584419

SN - 1055-7903

VL - 175

JO - Molecular Phylogenetics and Evolution

JF - Molecular Phylogenetics and Evolution

M1 - 107560

ER -

Recent speciation and phenotypic plasticity within a parthenogenetic lineage of levantine whip spiders (Chelicerata: Amblypygi: Charinidae)

Abstract

Bibliographical note

Keywords

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