Opening Pandora's box: Clitellum in phylogeny and taxonomy of earthworms

Tomá Pavlíček, Yarin Hadid, C. Csuzdi

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

The solution to the current contradictions in earthworm taxonomy and phylogeny is a better understanding of the underlying speciation process. The analysis of size and distribution of clitellar segments and that of tubercula pubertatis in the model homoploid genus Lumbricus provides prima facie evidence for the occurrence of the intra-chromosomal autohomoploid hybridization (autohomoploid hybridization = hybridization without changing the ploidy level and taking place between parents from the same panmictic population). The inferred principal mechanism of the autohomoploid hybridization is an unequal crossing recombining paralogous genes organized in a genomic island of divergence (called here "clitellar genomic island of divergence", CGID). Since clitellar segments constitute a prezygotic reproduction barrier and seem to correspond to the underlying genes at CGID on a one-to-one basis, their analysis helps to illuminate the underlying speciation process. The inferred characteristic features of the autohomoploid hybridization in earthworms are: (1) Presence of CGID; (2) Generation of quantitative changes in CGID leading to speciation by means of unequal crossing over (= separation of the process leading to speciation from the rest of genome); (3) Regulated distribution of breaking points; (4) Intra-lineage hybridizations, and (5) Homeotic character of the CGID genes. As far as we know, this is the first case of autohomoploid hybridization described in animals. Probably, it is not exaggerated to conclude that many earthworm evolutionary lineages (species) originated in the process of the described autohomploid hybridization in the CGID or in the process of inter-chromosomal duplications leading to polyploidization of the whole genome. We do not deny the possible existence of allopatric speciation in earthworms caused, for example, by established geographic or behavioural (e.g., assortative mating) barriers to inter-population gene flow. The major consequences of ignoring autohomoploid hybrid speciation in lumbricid earthworms (and presumably in other earthworm families as well) in phylogenetic analyses are: (i) Incorrect inference of phylogenies by applying bifurcating- like phylogenetic analysis instead of reticulate analyses as often seen in the low statistical supports for different clades in constructed bifurcating-like phylogenetic trees and for trees topologies (frequently not even tested). (ii) Misinterpretation of taxonomy and phylogeny by using genetic distance as the sole defining criterion.

Original languageEnglish
Pages (from-to)31-46
Number of pages16
JournalZoology in the Middle East
Volume58
DOIs
Publication statusPublished - 2012

Fingerprint

genomic islands
earthworms
hybridization
taxonomy
phylogeny
Lumbricus
allopatric speciation
genome
genes
assortative mating
crossing over
ploidy
topology
genetic distance
gene flow

Keywords

  • Clitellum
  • Erthworms
  • Hybridization
  • Lumbricus
  • Speciation
  • Tubercula pubertatis

ASJC Scopus subject areas

  • Animal Science and Zoology

Cite this

Opening Pandora's box : Clitellum in phylogeny and taxonomy of earthworms. / Pavlíček, Tomá; Hadid, Yarin; Csuzdi, C.

In: Zoology in the Middle East, Vol. 58, 2012, p. 31-46.

Research output: Contribution to journalArticle

@article{e2ec3eb7d05d457e9221a4de60ef6c8c,
title = "Opening Pandora's box: Clitellum in phylogeny and taxonomy of earthworms",
abstract = "The solution to the current contradictions in earthworm taxonomy and phylogeny is a better understanding of the underlying speciation process. The analysis of size and distribution of clitellar segments and that of tubercula pubertatis in the model homoploid genus Lumbricus provides prima facie evidence for the occurrence of the intra-chromosomal autohomoploid hybridization (autohomoploid hybridization = hybridization without changing the ploidy level and taking place between parents from the same panmictic population). The inferred principal mechanism of the autohomoploid hybridization is an unequal crossing recombining paralogous genes organized in a genomic island of divergence (called here {"}clitellar genomic island of divergence{"}, CGID). Since clitellar segments constitute a prezygotic reproduction barrier and seem to correspond to the underlying genes at CGID on a one-to-one basis, their analysis helps to illuminate the underlying speciation process. The inferred characteristic features of the autohomoploid hybridization in earthworms are: (1) Presence of CGID; (2) Generation of quantitative changes in CGID leading to speciation by means of unequal crossing over (= separation of the process leading to speciation from the rest of genome); (3) Regulated distribution of breaking points; (4) Intra-lineage hybridizations, and (5) Homeotic character of the CGID genes. As far as we know, this is the first case of autohomoploid hybridization described in animals. Probably, it is not exaggerated to conclude that many earthworm evolutionary lineages (species) originated in the process of the described autohomploid hybridization in the CGID or in the process of inter-chromosomal duplications leading to polyploidization of the whole genome. We do not deny the possible existence of allopatric speciation in earthworms caused, for example, by established geographic or behavioural (e.g., assortative mating) barriers to inter-population gene flow. The major consequences of ignoring autohomoploid hybrid speciation in lumbricid earthworms (and presumably in other earthworm families as well) in phylogenetic analyses are: (i) Incorrect inference of phylogenies by applying bifurcating- like phylogenetic analysis instead of reticulate analyses as often seen in the low statistical supports for different clades in constructed bifurcating-like phylogenetic trees and for trees topologies (frequently not even tested). (ii) Misinterpretation of taxonomy and phylogeny by using genetic distance as the sole defining criterion.",
keywords = "Clitellum, Erthworms, Hybridization, Lumbricus, Speciation, Tubercula pubertatis",
author = "Tom{\'a} Pavl{\'i}ček and Yarin Hadid and C. Csuzdi",
year = "2012",
doi = "10.1080/09397140.2012.10648983",
language = "English",
volume = "58",
pages = "31--46",
journal = "Zoology in the Middle East",
issn = "0939-7140",
publisher = "Max Kasparek Verlag",

}

TY - JOUR

T1 - Opening Pandora's box

T2 - Clitellum in phylogeny and taxonomy of earthworms

AU - Pavlíček, Tomá

AU - Hadid, Yarin

AU - Csuzdi, C.

PY - 2012

Y1 - 2012

N2 - The solution to the current contradictions in earthworm taxonomy and phylogeny is a better understanding of the underlying speciation process. The analysis of size and distribution of clitellar segments and that of tubercula pubertatis in the model homoploid genus Lumbricus provides prima facie evidence for the occurrence of the intra-chromosomal autohomoploid hybridization (autohomoploid hybridization = hybridization without changing the ploidy level and taking place between parents from the same panmictic population). The inferred principal mechanism of the autohomoploid hybridization is an unequal crossing recombining paralogous genes organized in a genomic island of divergence (called here "clitellar genomic island of divergence", CGID). Since clitellar segments constitute a prezygotic reproduction barrier and seem to correspond to the underlying genes at CGID on a one-to-one basis, their analysis helps to illuminate the underlying speciation process. The inferred characteristic features of the autohomoploid hybridization in earthworms are: (1) Presence of CGID; (2) Generation of quantitative changes in CGID leading to speciation by means of unequal crossing over (= separation of the process leading to speciation from the rest of genome); (3) Regulated distribution of breaking points; (4) Intra-lineage hybridizations, and (5) Homeotic character of the CGID genes. As far as we know, this is the first case of autohomoploid hybridization described in animals. Probably, it is not exaggerated to conclude that many earthworm evolutionary lineages (species) originated in the process of the described autohomploid hybridization in the CGID or in the process of inter-chromosomal duplications leading to polyploidization of the whole genome. We do not deny the possible existence of allopatric speciation in earthworms caused, for example, by established geographic or behavioural (e.g., assortative mating) barriers to inter-population gene flow. The major consequences of ignoring autohomoploid hybrid speciation in lumbricid earthworms (and presumably in other earthworm families as well) in phylogenetic analyses are: (i) Incorrect inference of phylogenies by applying bifurcating- like phylogenetic analysis instead of reticulate analyses as often seen in the low statistical supports for different clades in constructed bifurcating-like phylogenetic trees and for trees topologies (frequently not even tested). (ii) Misinterpretation of taxonomy and phylogeny by using genetic distance as the sole defining criterion.

AB - The solution to the current contradictions in earthworm taxonomy and phylogeny is a better understanding of the underlying speciation process. The analysis of size and distribution of clitellar segments and that of tubercula pubertatis in the model homoploid genus Lumbricus provides prima facie evidence for the occurrence of the intra-chromosomal autohomoploid hybridization (autohomoploid hybridization = hybridization without changing the ploidy level and taking place between parents from the same panmictic population). The inferred principal mechanism of the autohomoploid hybridization is an unequal crossing recombining paralogous genes organized in a genomic island of divergence (called here "clitellar genomic island of divergence", CGID). Since clitellar segments constitute a prezygotic reproduction barrier and seem to correspond to the underlying genes at CGID on a one-to-one basis, their analysis helps to illuminate the underlying speciation process. The inferred characteristic features of the autohomoploid hybridization in earthworms are: (1) Presence of CGID; (2) Generation of quantitative changes in CGID leading to speciation by means of unequal crossing over (= separation of the process leading to speciation from the rest of genome); (3) Regulated distribution of breaking points; (4) Intra-lineage hybridizations, and (5) Homeotic character of the CGID genes. As far as we know, this is the first case of autohomoploid hybridization described in animals. Probably, it is not exaggerated to conclude that many earthworm evolutionary lineages (species) originated in the process of the described autohomploid hybridization in the CGID or in the process of inter-chromosomal duplications leading to polyploidization of the whole genome. We do not deny the possible existence of allopatric speciation in earthworms caused, for example, by established geographic or behavioural (e.g., assortative mating) barriers to inter-population gene flow. The major consequences of ignoring autohomoploid hybrid speciation in lumbricid earthworms (and presumably in other earthworm families as well) in phylogenetic analyses are: (i) Incorrect inference of phylogenies by applying bifurcating- like phylogenetic analysis instead of reticulate analyses as often seen in the low statistical supports for different clades in constructed bifurcating-like phylogenetic trees and for trees topologies (frequently not even tested). (ii) Misinterpretation of taxonomy and phylogeny by using genetic distance as the sole defining criterion.

KW - Clitellum

KW - Erthworms

KW - Hybridization

KW - Lumbricus

KW - Speciation

KW - Tubercula pubertatis

UR - http://www.scopus.com/inward/record.url?scp=84911948653&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84911948653&partnerID=8YFLogxK

U2 - 10.1080/09397140.2012.10648983

DO - 10.1080/09397140.2012.10648983

M3 - Article

AN - SCOPUS:84911948653

VL - 58

SP - 31

EP - 46

JO - Zoology in the Middle East

JF - Zoology in the Middle East

SN - 0939-7140

ER -