Phylogeny of Merlin’s grass (Isoetaceae): revealing an “Amborella syndrome” and the importance of geographic distribution for understanding current and historical diversity

Abstract Background Merlin’s grass (Isoetes, Isoetaceae, Lycopsida), is the extant remnant of the isoetalean wood-producing lycopsids that originated during the Paleozoic, possibly in aquatic or boggy habitats. Modern day species are aquatic, semi-aquatic or terrestrial and occur almost worldwide. T...

Full description

Bibliographic Details
Main Authors: Eva Larsén, Niklas Wikström, Anbar Khodabandeh, Catarina Rydin
Format: Article
Language:English
Published: BMC 2022-03-01
Series:BMC Ecology and Evolution
Subjects:
Online Access:https://doi.org/10.1186/s12862-022-01988-w
_version_ 1818319716094050304
author Eva Larsén
Niklas Wikström
Anbar Khodabandeh
Catarina Rydin
author_facet Eva Larsén
Niklas Wikström
Anbar Khodabandeh
Catarina Rydin
author_sort Eva Larsén
collection DOAJ
description Abstract Background Merlin’s grass (Isoetes, Isoetaceae, Lycopsida), is the extant remnant of the isoetalean wood-producing lycopsids that originated during the Paleozoic, possibly in aquatic or boggy habitats. Modern day species are aquatic, semi-aquatic or terrestrial and occur almost worldwide. They display little morphological variation; the lobed corm has helically arranged leaves with internal air channels and basal sporangia. Genetic variation has also proven limited, which has hampered phylogenetic inference. We investigate evolutionary relationships in Isoetes, using molecular data and an extended sample of species compared to previous work, adding species that have never before been included in a phylogenetic study. Results Our results reveal an unexpected discovery of an “Amborella syndrome” in Isoetaceae: a single poorly known species is sister to the remaining family. The species, Isoetes wormaldii, is a rare endemic to the Eastern Cape of South Africa. Its leaves are flattened with a rounded point, which sharply contrasts with the awl-shaped leaves of most other species of Isoetes. The remaining species of Isoetes are resolved in five major clades, also indicated in previous work. While the phylogeny shows geographic structure, the patterns are complex. For example, tropical-southern African species occur in at least five clades, and Indian, Australian and Mediterranean species in at least three clades each. Conclusion The evolutionary and biogeographical history of Isoetes is not easily explained, and may conceivably include ample extinction and a mixture of ancient and more recent processes. Previously shown difficulties with node age estimation increase the problem. The here demonstrated sister-relationship between the phylogenetically, morphologically and genetically distinct Isoetes wormaldii and the remaining family appears to bridge the morphological gap between Isoetes and its extinct relatives, although further studies are needed. Moreover, it shortens the branch length to its living sister genus Selaginella, and may enhance node age estimation in future studies. Isoetes wormaldii is critically endangered, known only from one (to a few) minor populations. Immediate actions need to be taken if we want to prevent this unique species from going extinct.
first_indexed 2024-12-13T10:13:32Z
format Article
id doaj.art-efd91bf4402648b7aadd83d52bfa29a3
institution Directory Open Access Journal
issn 2730-7182
language English
last_indexed 2024-12-13T10:13:32Z
publishDate 2022-03-01
publisher BMC
record_format Article
series BMC Ecology and Evolution
spelling doaj.art-efd91bf4402648b7aadd83d52bfa29a32022-12-21T23:51:23ZengBMCBMC Ecology and Evolution2730-71822022-03-0122111710.1186/s12862-022-01988-wPhylogeny of Merlin’s grass (Isoetaceae): revealing an “Amborella syndrome” and the importance of geographic distribution for understanding current and historical diversityEva Larsén0Niklas Wikström1Anbar Khodabandeh2Catarina Rydin3Department of Ecology, Environment and Plant Sciences, Stockholm UniversityDepartment of Ecology, Environment and Plant Sciences, Stockholm UniversityDepartment of Ecology, Environment and Plant Sciences, Stockholm UniversityDepartment of Ecology, Environment and Plant Sciences, Stockholm UniversityAbstract Background Merlin’s grass (Isoetes, Isoetaceae, Lycopsida), is the extant remnant of the isoetalean wood-producing lycopsids that originated during the Paleozoic, possibly in aquatic or boggy habitats. Modern day species are aquatic, semi-aquatic or terrestrial and occur almost worldwide. They display little morphological variation; the lobed corm has helically arranged leaves with internal air channels and basal sporangia. Genetic variation has also proven limited, which has hampered phylogenetic inference. We investigate evolutionary relationships in Isoetes, using molecular data and an extended sample of species compared to previous work, adding species that have never before been included in a phylogenetic study. Results Our results reveal an unexpected discovery of an “Amborella syndrome” in Isoetaceae: a single poorly known species is sister to the remaining family. The species, Isoetes wormaldii, is a rare endemic to the Eastern Cape of South Africa. Its leaves are flattened with a rounded point, which sharply contrasts with the awl-shaped leaves of most other species of Isoetes. The remaining species of Isoetes are resolved in five major clades, also indicated in previous work. While the phylogeny shows geographic structure, the patterns are complex. For example, tropical-southern African species occur in at least five clades, and Indian, Australian and Mediterranean species in at least three clades each. Conclusion The evolutionary and biogeographical history of Isoetes is not easily explained, and may conceivably include ample extinction and a mixture of ancient and more recent processes. Previously shown difficulties with node age estimation increase the problem. The here demonstrated sister-relationship between the phylogenetically, morphologically and genetically distinct Isoetes wormaldii and the remaining family appears to bridge the morphological gap between Isoetes and its extinct relatives, although further studies are needed. Moreover, it shortens the branch length to its living sister genus Selaginella, and may enhance node age estimation in future studies. Isoetes wormaldii is critically endangered, known only from one (to a few) minor populations. Immediate actions need to be taken if we want to prevent this unique species from going extinct.https://doi.org/10.1186/s12862-022-01988-wEastern CapeIsoetesIsoetes wormaldiiPhylogenySpecies distributionDispersal
spellingShingle Eva Larsén
Niklas Wikström
Anbar Khodabandeh
Catarina Rydin
Phylogeny of Merlin’s grass (Isoetaceae): revealing an “Amborella syndrome” and the importance of geographic distribution for understanding current and historical diversity
BMC Ecology and Evolution
Eastern Cape
Isoetes
Isoetes wormaldii
Phylogeny
Species distribution
Dispersal
title Phylogeny of Merlin’s grass (Isoetaceae): revealing an “Amborella syndrome” and the importance of geographic distribution for understanding current and historical diversity
title_full Phylogeny of Merlin’s grass (Isoetaceae): revealing an “Amborella syndrome” and the importance of geographic distribution for understanding current and historical diversity
title_fullStr Phylogeny of Merlin’s grass (Isoetaceae): revealing an “Amborella syndrome” and the importance of geographic distribution for understanding current and historical diversity
title_full_unstemmed Phylogeny of Merlin’s grass (Isoetaceae): revealing an “Amborella syndrome” and the importance of geographic distribution for understanding current and historical diversity
title_short Phylogeny of Merlin’s grass (Isoetaceae): revealing an “Amborella syndrome” and the importance of geographic distribution for understanding current and historical diversity
title_sort phylogeny of merlin s grass isoetaceae revealing an amborella syndrome and the importance of geographic distribution for understanding current and historical diversity
topic Eastern Cape
Isoetes
Isoetes wormaldii
Phylogeny
Species distribution
Dispersal
url https://doi.org/10.1186/s12862-022-01988-w
work_keys_str_mv AT evalarsen phylogenyofmerlinsgrassisoetaceaerevealinganamborellasyndromeandtheimportanceofgeographicdistributionforunderstandingcurrentandhistoricaldiversity
AT niklaswikstrom phylogenyofmerlinsgrassisoetaceaerevealinganamborellasyndromeandtheimportanceofgeographicdistributionforunderstandingcurrentandhistoricaldiversity
AT anbarkhodabandeh phylogenyofmerlinsgrassisoetaceaerevealinganamborellasyndromeandtheimportanceofgeographicdistributionforunderstandingcurrentandhistoricaldiversity
AT catarinarydin phylogenyofmerlinsgrassisoetaceaerevealinganamborellasyndromeandtheimportanceofgeographicdistributionforunderstandingcurrentandhistoricaldiversity