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Molecular phylogeny of the phytoparasitic mite family Phytoptidae (Acariformes: Eriophyoidea) identified the female genitalic anatomy as a major macroevolutionary factor and revealed multiple origins of gall induction

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Authors
Chetverikov, Philipp
Craemer, Charnie
Cvrković, Tatjana
Klimov, Pavel
Petanović, Radmila
Romanovich, Anna
Sukhareva, Sogdiana
Zukoff, Sarah
Bolton, Samuel
Amrine, James
Article (Published version)
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Abstract
Phytoptidae s.str. is a lineage of eriophyoid mites associated with angiosperms. Based on representative taxon sampling and four gene markers (COI, HSP70, 18S, and 28S), we inferred the molecular phylogeny of this group and performed comparative analyses of cuticle-lined female internal genitalia. Although basal relationships were unclear, several well supported clades were recovered. These clades were supported by geography, host associations, and female genital anatomy, but contradicted the current morphology-based systematics. The monophyly of each of five conventional supraspecific groupings (Fragariocoptes, Phytoptus, Phytoptinae, Sierraphytoptinae, and Sierraphytoptini) is rejected based on a series of statistical tests. Additionally, four morphological characters (the absence of tibial solenidion φ and opisthosomal seta c1, presence of telosomal pseudotagma, and ‘morphotype’) were found to be homoplasies that cannot be used to confidently delimit supraspecific lineages of phytop...tids. However, our molecular topology was highly congruent with female genital characters. Eight molecular clades were unambiguously supported by the shapes and topography of the spermathecal apparatus and genital apodemes. This suggests that the female genital anatomy could be an important factor affecting cladogenesis in Phytoptidae, a conclusion contrasting with the general expectation that host characteristics should be a major macroevolutionary force influencing the evolution of host-specific symbionts. Indeed, despite the high host-specificity, there were no apparent cophylogenetic patterns. Furthermore, we show that gall-inducing ability evolved multiple times in phytoptids. Because gall formation creates nearly instantaneous niche partitioning and the potential loss or reduction of gene flow, we hypothesize that it could be an important evolutionary factor affecting speciation within different host-associated clades of phytoptid mites.

Source:
Experimental and Applied Acarology, 2021, 83, 1, 31-68
Publisher:
  • Springer
Funding / projects:
  • Russian Science Foundation (Project 19-14-00004)
  • Russian Foundation for Basic Research (RFBR grant # 19-04-00127 A)
  • Research projects of ZIN RAS (AAAA-A19-119020790133-6)
  • The Serbian Academy of Sciences and Arts (project F-195)
  • St. Petersburg State University (project INI_2018-3 # 49711063)

DOI: 10.1007/s10493-020-00571-6

ISSN: 1572-9702; 0168-8162

WoS: 000590204100001

Scopus: 2-s2.0-85096110461
[ Google Scholar ]
11
3
URI
https://plantarum.izbis.bg.ac.rs/handle/123456789/708
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  • Radovi istraživača / Researchers' publications
Institution/Community
IZBIS
TY  - JOUR
AU  - Chetverikov, Philipp
AU  - Craemer, Charnie
AU  - Cvrković, Tatjana
AU  - Klimov, Pavel
AU  - Petanović, Radmila
AU  - Romanovich, Anna
AU  - Sukhareva, Sogdiana
AU  - Zukoff, Sarah
AU  - Bolton, Samuel
AU  - Amrine, James
PY  - 2021
UR  - https://plantarum.izbis.bg.ac.rs/handle/123456789/708
AB  - Phytoptidae s.str. is a lineage of eriophyoid mites associated with angiosperms. Based on representative taxon sampling and four gene markers (COI, HSP70, 18S, and 28S), we inferred the molecular phylogeny of this group and performed comparative analyses of cuticle-lined female internal genitalia. Although basal relationships were unclear, several well supported clades were recovered. These clades were supported by geography, host associations, and female genital anatomy, but contradicted the current morphology-based systematics. The monophyly of each of five conventional supraspecific groupings (Fragariocoptes, Phytoptus, Phytoptinae, Sierraphytoptinae, and Sierraphytoptini) is rejected based on a series of statistical tests. Additionally, four morphological characters (the absence of tibial solenidion φ and opisthosomal seta c1, presence of telosomal pseudotagma, and ‘morphotype’) were found to be homoplasies that cannot be used to confidently delimit supraspecific lineages of phytoptids. However, our molecular topology was highly congruent with female genital characters. Eight molecular clades were unambiguously supported by the shapes and topography of the spermathecal apparatus and genital apodemes. This suggests that the female genital anatomy could be an important factor affecting cladogenesis in Phytoptidae, a conclusion contrasting with the general expectation that host characteristics should be a major macroevolutionary force influencing the evolution of host-specific symbionts. Indeed, despite the high host-specificity, there were no apparent cophylogenetic patterns. Furthermore, we show that gall-inducing ability evolved multiple times in phytoptids. Because gall formation creates nearly instantaneous niche partitioning and the potential loss or reduction of gene flow, we hypothesize that it could be an important evolutionary factor affecting speciation within different host-associated clades of phytoptid mites.
PB  - Springer
T2  - Experimental and Applied Acarology
T1  - Molecular phylogeny of the phytoparasitic mite family Phytoptidae (Acariformes: Eriophyoidea) identified the female genitalic anatomy as a major macroevolutionary factor and revealed multiple origins of gall induction
EP  - 68
IS  - 1
SP  - 31
VL  - 83
DO  - 10.1007/s10493-020-00571-6
ER  - 
@article{
author = "Chetverikov, Philipp and Craemer, Charnie and Cvrković, Tatjana and Klimov, Pavel and Petanović, Radmila and Romanovich, Anna and Sukhareva, Sogdiana and Zukoff, Sarah and Bolton, Samuel and Amrine, James",
year = "2021",
abstract = "Phytoptidae s.str. is a lineage of eriophyoid mites associated with angiosperms. Based on representative taxon sampling and four gene markers (COI, HSP70, 18S, and 28S), we inferred the molecular phylogeny of this group and performed comparative analyses of cuticle-lined female internal genitalia. Although basal relationships were unclear, several well supported clades were recovered. These clades were supported by geography, host associations, and female genital anatomy, but contradicted the current morphology-based systematics. The monophyly of each of five conventional supraspecific groupings (Fragariocoptes, Phytoptus, Phytoptinae, Sierraphytoptinae, and Sierraphytoptini) is rejected based on a series of statistical tests. Additionally, four morphological characters (the absence of tibial solenidion φ and opisthosomal seta c1, presence of telosomal pseudotagma, and ‘morphotype’) were found to be homoplasies that cannot be used to confidently delimit supraspecific lineages of phytoptids. However, our molecular topology was highly congruent with female genital characters. Eight molecular clades were unambiguously supported by the shapes and topography of the spermathecal apparatus and genital apodemes. This suggests that the female genital anatomy could be an important factor affecting cladogenesis in Phytoptidae, a conclusion contrasting with the general expectation that host characteristics should be a major macroevolutionary force influencing the evolution of host-specific symbionts. Indeed, despite the high host-specificity, there were no apparent cophylogenetic patterns. Furthermore, we show that gall-inducing ability evolved multiple times in phytoptids. Because gall formation creates nearly instantaneous niche partitioning and the potential loss or reduction of gene flow, we hypothesize that it could be an important evolutionary factor affecting speciation within different host-associated clades of phytoptid mites.",
publisher = "Springer",
journal = "Experimental and Applied Acarology",
title = "Molecular phylogeny of the phytoparasitic mite family Phytoptidae (Acariformes: Eriophyoidea) identified the female genitalic anatomy as a major macroevolutionary factor and revealed multiple origins of gall induction",
pages = "68-31",
number = "1",
volume = "83",
doi = "10.1007/s10493-020-00571-6"
}
Chetverikov, P., Craemer, C., Cvrković, T., Klimov, P., Petanović, R., Romanovich, A., Sukhareva, S., Zukoff, S., Bolton, S.,& Amrine, J.. (2021). Molecular phylogeny of the phytoparasitic mite family Phytoptidae (Acariformes: Eriophyoidea) identified the female genitalic anatomy as a major macroevolutionary factor and revealed multiple origins of gall induction. in Experimental and Applied Acarology
Springer., 83(1), 31-68.
https://doi.org/10.1007/s10493-020-00571-6
Chetverikov P, Craemer C, Cvrković T, Klimov P, Petanović R, Romanovich A, Sukhareva S, Zukoff S, Bolton S, Amrine J. Molecular phylogeny of the phytoparasitic mite family Phytoptidae (Acariformes: Eriophyoidea) identified the female genitalic anatomy as a major macroevolutionary factor and revealed multiple origins of gall induction. in Experimental and Applied Acarology. 2021;83(1):31-68.
doi:10.1007/s10493-020-00571-6 .
Chetverikov, Philipp, Craemer, Charnie, Cvrković, Tatjana, Klimov, Pavel, Petanović, Radmila, Romanovich, Anna, Sukhareva, Sogdiana, Zukoff, Sarah, Bolton, Samuel, Amrine, James, "Molecular phylogeny of the phytoparasitic mite family Phytoptidae (Acariformes: Eriophyoidea) identified the female genitalic anatomy as a major macroevolutionary factor and revealed multiple origins of gall induction" in Experimental and Applied Acarology, 83, no. 1 (2021):31-68,
https://doi.org/10.1007/s10493-020-00571-6 . .

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