The chicken or the egg? Adaptation to desiccation and salinity tolerance in a lineage of water beetles

Transitions from fresh to saline habitats are restricted to a handful of insect lineages, as the colonization of saline waters requires specialized mechanisms to deal with osmotic stress. Previous studies have suggested that tolerance to salinity and desiccation could be mechanistically and evolutionarily linked, but the temporal sequence of these adaptations is not well established for individual lineages. We combined molecular, physiological and ecological data to explore the evolution of desiccation resistance, hyporegulation ability (i.e., the ability to osmoregulate in hyperosmotic media) and habitat transitions in the water beetle genus Enochrus subgenus Lumetus (Hydrophilidae). We tested whether enhanced desiccation resistance evolved before increases in hyporegulation ability or vice versa, or whether the two mechanisms evolved in parallel. The most recent ancestor of Lumetus was inferred to have high desiccation resistance and moderate hyporegulation ability. There were repeated shifts between habitats with differing levels of salinity in the radiation of the group, those to the most saline habitats generally occurring more rapidly than those to less saline ones. Significant and accelerated changes in hyporegulation ability evolved in parallel with smaller and more progressive increases in desiccation resistance across the phylogeny, associated with the colonization of meso‐ and hypersaline waters during global aridification events. All species with high hyporegulation ability were also desiccation‐resistant, but not vice versa. Overall, results are consistent with the hypothesis that desiccation resistance mechanisms evolved first and provided the physiological basis for the development of hyporegulation ability, allowing these insects to colonize and diversify across meso‐ and hypersaline habitats.

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Bibliographic Details
Main Authors: Pallarés, Susana, Arribas, Paula, Bilton, David T., Millán, Andrés, Velasco, Josefa, Ribera, Ignacio
Other Authors: Ministerio de Economía y Competitividad (España)
Format: artículo biblioteca
Published: John Wiley & Sons 2017-10
Subjects:Ancestral reconstruction, Hyporegulation ability, Water loss, Inland saline waters, Habitat transitions, Aquatic insects,
Online Access:http://hdl.handle.net/10261/185003
http://dx.doi.org/10.13039/501100004687
http://dx.doi.org/10.13039/501100000288
http://dx.doi.org/10.13039/501100003329
http://dx.doi.org/10.13039/501100000780
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spelling dig-ipna-es-10261-1850032022-10-27T10:27:52Z The chicken or the egg? Adaptation to desiccation and salinity tolerance in a lineage of water beetles Pallarés, Susana Arribas, Paula Bilton, David T. Millán, Andrés Velasco, Josefa Ribera, Ignacio Ministerio de Economía y Competitividad (España) Royal Society (UK) Universidad de Murcia European Commission Ancestral reconstruction Hyporegulation ability Water loss Inland saline waters Habitat transitions Aquatic insects Transitions from fresh to saline habitats are restricted to a handful of insect lineages, as the colonization of saline waters requires specialized mechanisms to deal with osmotic stress. Previous studies have suggested that tolerance to salinity and desiccation could be mechanistically and evolutionarily linked, but the temporal sequence of these adaptations is not well established for individual lineages. We combined molecular, physiological and ecological data to explore the evolution of desiccation resistance, hyporegulation ability (i.e., the ability to osmoregulate in hyperosmotic media) and habitat transitions in the water beetle genus Enochrus subgenus Lumetus (Hydrophilidae). We tested whether enhanced desiccation resistance evolved before increases in hyporegulation ability or vice versa, or whether the two mechanisms evolved in parallel. The most recent ancestor of Lumetus was inferred to have high desiccation resistance and moderate hyporegulation ability. There were repeated shifts between habitats with differing levels of salinity in the radiation of the group, those to the most saline habitats generally occurring more rapidly than those to less saline ones. Significant and accelerated changes in hyporegulation ability evolved in parallel with smaller and more progressive increases in desiccation resistance across the phylogeny, associated with the colonization of meso‐ and hypersaline waters during global aridification events. All species with high hyporegulation ability were also desiccation‐resistant, but not vice versa. Overall, results are consistent with the hypothesis that desiccation resistance mechanisms evolved first and provided the physiological basis for the development of hyporegulation ability, allowing these insects to colonize and diversify across meso‐ and hypersaline habitats. This work was funded by the I+D+i project CGL2013‐48950‐C2‐1&2‐P (AEI/FEDER, UE), a predoctoral grant and a scholarship grant from the University of Murcia to S. Pallarés and two postdoctoral grants from the Royal Society UK (Newton International Program) and from the Spanish Ministry of Economy and Competitivity (Juan de la Cierva Formación Program) to P. Arribas. Peer reviewed Peer Reviewed 2019-06-27T12:57:01Z 2019-06-27T12:57:01Z 2017-10 2019-06-27T12:57:01Z artículo http://purl.org/coar/resource_type/c_6501 Molecular Ecology 26(20): 5614-5628 (2017) 0962-1083 http://hdl.handle.net/10261/185003 10.1111/mec.14334 1365-294X http://dx.doi.org/10.13039/501100004687 http://dx.doi.org/10.13039/501100000288 http://dx.doi.org/10.13039/501100003329 http://dx.doi.org/10.13039/501100000780 #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/CGL2013‐48950‐C2‐1-P info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/CGL2013‐48950‐C2‐2‐P Pallarés, Susana; Arribas, Paula ; Bilton, David T.; Millán, Andrés; Velasco, Josefa; Ribera, Ignacio (2017): Data from: The chicken or the egg? Adaptation to desiccation and salinity tolerance in a lineage of water beetles [Dataset]; Dryad; Version 1; https://doi.org/10.5061/dryad.2j3c8 https://doi.org/10.1111/mec.14334 Sí none John Wiley & Sons
institution IPNA ES
collection DSpace
country España
countrycode ES
component Bibliográfico
access En linea
databasecode dig-ipna-es
tag biblioteca
region Europa del Sur
libraryname Biblioteca del IPNA España
topic Ancestral reconstruction
Hyporegulation ability
Water loss
Inland saline waters
Habitat transitions
Aquatic insects
Ancestral reconstruction
Hyporegulation ability
Water loss
Inland saline waters
Habitat transitions
Aquatic insects
spellingShingle Ancestral reconstruction
Hyporegulation ability
Water loss
Inland saline waters
Habitat transitions
Aquatic insects
Ancestral reconstruction
Hyporegulation ability
Water loss
Inland saline waters
Habitat transitions
Aquatic insects
Pallarés, Susana
Arribas, Paula
Bilton, David T.
Millán, Andrés
Velasco, Josefa
Ribera, Ignacio
The chicken or the egg? Adaptation to desiccation and salinity tolerance in a lineage of water beetles
description Transitions from fresh to saline habitats are restricted to a handful of insect lineages, as the colonization of saline waters requires specialized mechanisms to deal with osmotic stress. Previous studies have suggested that tolerance to salinity and desiccation could be mechanistically and evolutionarily linked, but the temporal sequence of these adaptations is not well established for individual lineages. We combined molecular, physiological and ecological data to explore the evolution of desiccation resistance, hyporegulation ability (i.e., the ability to osmoregulate in hyperosmotic media) and habitat transitions in the water beetle genus Enochrus subgenus Lumetus (Hydrophilidae). We tested whether enhanced desiccation resistance evolved before increases in hyporegulation ability or vice versa, or whether the two mechanisms evolved in parallel. The most recent ancestor of Lumetus was inferred to have high desiccation resistance and moderate hyporegulation ability. There were repeated shifts between habitats with differing levels of salinity in the radiation of the group, those to the most saline habitats generally occurring more rapidly than those to less saline ones. Significant and accelerated changes in hyporegulation ability evolved in parallel with smaller and more progressive increases in desiccation resistance across the phylogeny, associated with the colonization of meso‐ and hypersaline waters during global aridification events. All species with high hyporegulation ability were also desiccation‐resistant, but not vice versa. Overall, results are consistent with the hypothesis that desiccation resistance mechanisms evolved first and provided the physiological basis for the development of hyporegulation ability, allowing these insects to colonize and diversify across meso‐ and hypersaline habitats.
author2 Ministerio de Economía y Competitividad (España)
author_facet Ministerio de Economía y Competitividad (España)
Pallarés, Susana
Arribas, Paula
Bilton, David T.
Millán, Andrés
Velasco, Josefa
Ribera, Ignacio
format artículo
topic_facet Ancestral reconstruction
Hyporegulation ability
Water loss
Inland saline waters
Habitat transitions
Aquatic insects
author Pallarés, Susana
Arribas, Paula
Bilton, David T.
Millán, Andrés
Velasco, Josefa
Ribera, Ignacio
author_sort Pallarés, Susana
title The chicken or the egg? Adaptation to desiccation and salinity tolerance in a lineage of water beetles
title_short The chicken or the egg? Adaptation to desiccation and salinity tolerance in a lineage of water beetles
title_full The chicken or the egg? Adaptation to desiccation and salinity tolerance in a lineage of water beetles
title_fullStr The chicken or the egg? Adaptation to desiccation and salinity tolerance in a lineage of water beetles
title_full_unstemmed The chicken or the egg? Adaptation to desiccation and salinity tolerance in a lineage of water beetles
title_sort chicken or the egg? adaptation to desiccation and salinity tolerance in a lineage of water beetles
publisher John Wiley & Sons
publishDate 2017-10
url http://hdl.handle.net/10261/185003
http://dx.doi.org/10.13039/501100004687
http://dx.doi.org/10.13039/501100000288
http://dx.doi.org/10.13039/501100003329
http://dx.doi.org/10.13039/501100000780
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