Spiralian phylogeny informs the evolution of microscopic lineages

Christopher E. Laumer; Nicolas Tarik Bekkouche; Alexandra Kerbl; Freya Goetz; Ricardo C. Neves; Martin Vinther Sørensen; Reinhardt Møbjerg Kristensen; Andreas Hejnol; Casey W. Dunn; Gonzalo Giribet; Katrine Worsaae

doi:10.1016/j.cub.2015.06.068

Spiralian phylogeny informs the evolution of microscopic lineages

Christopher E. Laumer, Nicolas Tarik Bekkouche, Alexandra Kerbl, Freya Goetz, Ricardo C. Neves, Martin Vinther Sørensen, Reinhardt Møbjerg Kristensen, Andreas Hejnol, Casey W. Dunn, Gonzalo Giribet, Katrine Worsaae

Marine Biology

153 Citations (Scopus)

Abstract

Despite rapid advances in the study of metazoan evolutionary history [1], phylogenomic analyses have so far neglected a number of microscopic lineages that possess a unique combination of characters and are thus informative for our understanding of morphological evolution. Chief among these lineages are the recently described animal groups Micrognathozoa and Loricifera, as well as the two interstitial "Problematica" Diurodrilus and Lobatocerebrum [2]. These genera show a certain resemblance to Annelida in their cuticle and gut [3, 4]; however, both lack primary annelid characters such as segmentation and chaetae [5]. Moreover, they show unique features such as an inverted body-wall musculature or a novel pharyngeal organ. This and their ciliated epidermis have led some to propose relationships with other microscopic spiralians, namely Platyhelminthes, Gastrotricha, and in the case of Diurodrilus, with Micrognathozoa [6, 7] - lineages that are grouped by some analyses into "Platyzoa," a clade whose status remains uncertain [1, 8-11]. Here, we assess the interrelationships among the meiofaunal and macrofaunal members of Spiralia using 402 orthologs mined from genome and transcriptome assemblies of 90 taxa. Lobatocerebrum and Diurodrilus are found to be deeply nested members of Annelida, and unequivocal support is found for Micrognathozoa as the sister group of Rotifera. Analyses using site-heterogeneous substitution models further recover a lophophorate clade and position Loricifera + Priapulida as sister group to the remaining Ecdysozoa. Finally, with several meiofaunal lineages branching off early in the diversification of Spiralia, the emerging concept of a microscopic, acoelomate, direct-developing ancestor of Spiralia is reviewed.

Original language	English
Journal	Current Biology
Volume	25
Issue number	15
Pages (from-to)	2000-2006
Number of pages	7
ISSN	0960-9822
DOIs	https://doi.org/10.1016/j.cub.2015.06.068
Publication status	Published - 3 Aug 2015

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@article{153cf952879e4332bf81d2d7138d9640,

title = "Spiralian phylogeny informs the evolution of microscopic lineages",

abstract = "Despite rapid advances in the study of metazoan evolutionary history [1], phylogenomic analyses have so far neglected a number of microscopic lineages that possess a unique combination of characters and are thus informative for our understanding of morphological evolution. Chief among these lineages are the recently described animal groups Micrognathozoa and Loricifera, as well as the two interstitial {"}Problematica{"} Diurodrilus and Lobatocerebrum [2]. These genera show a certain resemblance to Annelida in their cuticle and gut [3, 4]; however, both lack primary annelid characters such as segmentation and chaetae [5]. Moreover, they show unique features such as an inverted body-wall musculature or a novel pharyngeal organ. This and their ciliated epidermis have led some to propose relationships with other microscopic spiralians, namely Platyhelminthes, Gastrotricha, and in the case of Diurodrilus, with Micrognathozoa [6, 7] - lineages that are grouped by some analyses into {"}Platyzoa,{"} a clade whose status remains uncertain [1, 8-11]. Here, we assess the interrelationships among the meiofaunal and macrofaunal members of Spiralia using 402 orthologs mined from genome and transcriptome assemblies of 90 taxa. Lobatocerebrum and Diurodrilus are found to be deeply nested members of Annelida, and unequivocal support is found for Micrognathozoa as the sister group of Rotifera. Analyses using site-heterogeneous substitution models further recover a lophophorate clade and position Loricifera + Priapulida as sister group to the remaining Ecdysozoa. Finally, with several meiofaunal lineages branching off early in the diversification of Spiralia, the emerging concept of a microscopic, acoelomate, direct-developing ancestor of Spiralia is reviewed.",

author = "Laumer, {Christopher E.} and Bekkouche, {Nicolas Tarik} and Alexandra Kerbl and Freya Goetz and Neves, {Ricardo C.} and S{\o}rensen, {Martin Vinther} and Kristensen, {Reinhardt M{\o}bjerg} and Andreas Hejnol and Dunn, {Casey W.} and Gonzalo Giribet and Katrine Worsaae",

year = "2015",

month = aug,

day = "3",

doi = "10.1016/j.cub.2015.06.068",

language = "English",

volume = "25",

pages = "2000--2006",

journal = "Current Biology",

issn = "0960-9822",

publisher = "Cell Press",

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TY - JOUR

T1 - Spiralian phylogeny informs the evolution of microscopic lineages

AU - Laumer, Christopher E.

AU - Bekkouche, Nicolas Tarik

AU - Kerbl, Alexandra

AU - Goetz, Freya

AU - Neves, Ricardo C.

AU - Sørensen, Martin Vinther

AU - Kristensen, Reinhardt Møbjerg

AU - Hejnol, Andreas

AU - Dunn, Casey W.

AU - Giribet, Gonzalo

AU - Worsaae, Katrine

PY - 2015/8/3

Y1 - 2015/8/3

N2 - Despite rapid advances in the study of metazoan evolutionary history [1], phylogenomic analyses have so far neglected a number of microscopic lineages that possess a unique combination of characters and are thus informative for our understanding of morphological evolution. Chief among these lineages are the recently described animal groups Micrognathozoa and Loricifera, as well as the two interstitial "Problematica" Diurodrilus and Lobatocerebrum [2]. These genera show a certain resemblance to Annelida in their cuticle and gut [3, 4]; however, both lack primary annelid characters such as segmentation and chaetae [5]. Moreover, they show unique features such as an inverted body-wall musculature or a novel pharyngeal organ. This and their ciliated epidermis have led some to propose relationships with other microscopic spiralians, namely Platyhelminthes, Gastrotricha, and in the case of Diurodrilus, with Micrognathozoa [6, 7] - lineages that are grouped by some analyses into "Platyzoa," a clade whose status remains uncertain [1, 8-11]. Here, we assess the interrelationships among the meiofaunal and macrofaunal members of Spiralia using 402 orthologs mined from genome and transcriptome assemblies of 90 taxa. Lobatocerebrum and Diurodrilus are found to be deeply nested members of Annelida, and unequivocal support is found for Micrognathozoa as the sister group of Rotifera. Analyses using site-heterogeneous substitution models further recover a lophophorate clade and position Loricifera + Priapulida as sister group to the remaining Ecdysozoa. Finally, with several meiofaunal lineages branching off early in the diversification of Spiralia, the emerging concept of a microscopic, acoelomate, direct-developing ancestor of Spiralia is reviewed.

AB - Despite rapid advances in the study of metazoan evolutionary history [1], phylogenomic analyses have so far neglected a number of microscopic lineages that possess a unique combination of characters and are thus informative for our understanding of morphological evolution. Chief among these lineages are the recently described animal groups Micrognathozoa and Loricifera, as well as the two interstitial "Problematica" Diurodrilus and Lobatocerebrum [2]. These genera show a certain resemblance to Annelida in their cuticle and gut [3, 4]; however, both lack primary annelid characters such as segmentation and chaetae [5]. Moreover, they show unique features such as an inverted body-wall musculature or a novel pharyngeal organ. This and their ciliated epidermis have led some to propose relationships with other microscopic spiralians, namely Platyhelminthes, Gastrotricha, and in the case of Diurodrilus, with Micrognathozoa [6, 7] - lineages that are grouped by some analyses into "Platyzoa," a clade whose status remains uncertain [1, 8-11]. Here, we assess the interrelationships among the meiofaunal and macrofaunal members of Spiralia using 402 orthologs mined from genome and transcriptome assemblies of 90 taxa. Lobatocerebrum and Diurodrilus are found to be deeply nested members of Annelida, and unequivocal support is found for Micrognathozoa as the sister group of Rotifera. Analyses using site-heterogeneous substitution models further recover a lophophorate clade and position Loricifera + Priapulida as sister group to the remaining Ecdysozoa. Finally, with several meiofaunal lineages branching off early in the diversification of Spiralia, the emerging concept of a microscopic, acoelomate, direct-developing ancestor of Spiralia is reviewed.

U2 - 10.1016/j.cub.2015.06.068

DO - 10.1016/j.cub.2015.06.068

M3 - Journal article

C2 - 26212884

SN - 0960-9822

VL - 25

SP - 2000

EP - 2006

JO - Current Biology

JF - Current Biology

IS - 15

ER -

Spiralian phylogeny informs the evolution of microscopic lineages

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