The neoteny goldilocks zone: The evolution of neoteny in <i>Ambystoma</i>

Lyons, Thomas; Arbuckle, Kevin

doi:10.1002/ece3.11240

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The neoteny goldilocks zone: The evolution of neoteny in <i>Ambystoma</i>

Thomas Lyons, Kevin Arbuckle

Ecology and Evolution, Volume: 14, Issue: 4

Swansea University Authors: Thomas Lyons, Kevin Arbuckle

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DOI (Published version): 10.1002/ece3.11240

Abstract

Neoteny is a developmental strategy wherein an organism reaches sexual maturity without associated adult characteristics. In salamanders, neoteny takes the form of individuals retaining aquatic larval characteristics such as external gills upon maturation. Mole salamanders (Ambystoma) occupy a wide...

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Published in:	Ecology and Evolution
ISSN:	2045-7758 2045-7758
Published:	Wiley 2024
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URI:	https://cronfa.swan.ac.uk/Record/cronfa66045
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In salamanders, neoteny takes the form of individuals retaining aquatic larval characteristics such as external gills upon maturation. Mole salamanders (Ambystoma) occupy a wide range of habitats and areas across the North American continent, and display examples of non-neotenic, facultatively neotenic and obligate neotenic species, providing high variation for investigating the factors influencing the evolution of neoteny. Here, we use phylogenetic comparative methods to test existing hypotheses that neoteny is associated with elevational and latitudinal distribution, cave-associated isolation, and hybridisation-related polyploidy. We also test if neoteny influences the diversity of habitats a species can occupy, since the restriction to an aquatic life should constrain the availability of different niches. We find that neoteny tends to occur in a narrow latitudinal band between 20–30° North, with particularly narrow latitudinal ranges for obligate compared to facultative neotenic species (16–52° North). We also find that facultatively neotenic species occur at elevations more than twice as high as other species on average, and that species with a higher frequency of neoteny typically have lower habitat diversity. Our results suggest that evolutionary transitions between non-neotenic and facultative neoteny states occur at relatively high and approximately equal rates. Moreover, we estimate that obligate neoteny cannot evolve directly from non-neotenic species (and vice versa), such that facultative neoteny acts as an evolutionary ‘stepping stone’ to and from obligate neoteny. However, our transition rate estimates suggest that obligate neoteny is lost >4-times faster than it evolves, partly explaining the rarity of obligate species. 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spelling	v2 66045 2024-04-11 The neoteny goldilocks zone: The evolution of neoteny in <i>Ambystoma</i> d6cc03a9dd7ef442d82d66f114c9ae58 Thomas Lyons Thomas Lyons true false d1775d20b12e430869cc7be5d7d4a27e 0000-0002-9171-5874 Kevin Arbuckle Kevin Arbuckle true false 2024-04-11 BGPS Neoteny is a developmental strategy wherein an organism reaches sexual maturity without associated adult characteristics. In salamanders, neoteny takes the form of individuals retaining aquatic larval characteristics such as external gills upon maturation. Mole salamanders (Ambystoma) occupy a wide range of habitats and areas across the North American continent, and display examples of non-neotenic, facultatively neotenic and obligate neotenic species, providing high variation for investigating the factors influencing the evolution of neoteny. Here, we use phylogenetic comparative methods to test existing hypotheses that neoteny is associated with elevational and latitudinal distribution, cave-associated isolation, and hybridisation-related polyploidy. We also test if neoteny influences the diversity of habitats a species can occupy, since the restriction to an aquatic life should constrain the availability of different niches. We find that neoteny tends to occur in a narrow latitudinal band between 20–30° North, with particularly narrow latitudinal ranges for obligate compared to facultative neotenic species (16–52° North). We also find that facultatively neotenic species occur at elevations more than twice as high as other species on average, and that species with a higher frequency of neoteny typically have lower habitat diversity. Our results suggest that evolutionary transitions between non-neotenic and facultative neoteny states occur at relatively high and approximately equal rates. Moreover, we estimate that obligate neoteny cannot evolve directly from non-neotenic species (and vice versa), such that facultative neoteny acts as an evolutionary ‘stepping stone’ to and from obligate neoteny. However, our transition rate estimates suggest that obligate neoteny is lost >4-times faster than it evolves, partly explaining the rarity of obligate species. These results support the hypothesis that low latitudes favour the evolution of neoteny, presumably linked to more stable (aquatic) environments due to reduced seasonality, but once evolved it may constrain the diversity of habitats. Journal Article Ecology and Evolution 14 4 Wiley 2045-7758 2045-7758 amphibian ecology, axolotl, life history evolution, Paedomorphosis, phylogenetic comparativemethods 8 4 2024 2024-04-08 10.1002/ece3.11240 COLLEGE NANME Biosciences Geography and Physics School COLLEGE CODE BGPS Swansea University SU Library paid the OA fee (TA Institutional Deal) Swansea University 2024-06-03T11:59:55.5737223 2024-04-11T17:12:27.2800008 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences Thomas Lyons 1 Kevin Arbuckle 0000-0002-9171-5874 2 66045__30004__f09b09069c8e4c438e9a27118a481c93.pdf neoteny goldilocks zone - the evolution of neoteny in ambystoma.pdf 2024-04-11T17:15:08.1194955 Output 2394146 application/pdf Version of Record true © 2024 The Authors. This is an open access article under the terms of the Creative Commons Attribution License. true eng http://creativecommons.org/licenses/by/4.0/
title	The neoteny goldilocks zone: The evolution of neoteny in <i>Ambystoma</i>
spellingShingle	The neoteny goldilocks zone: The evolution of neoteny in <i>Ambystoma</i> Thomas Lyons Kevin Arbuckle
title_short	The neoteny goldilocks zone: The evolution of neoteny in <i>Ambystoma</i>
title_full	The neoteny goldilocks zone: The evolution of neoteny in <i>Ambystoma</i>
title_fullStr	The neoteny goldilocks zone: The evolution of neoteny in <i>Ambystoma</i>
title_full_unstemmed	The neoteny goldilocks zone: The evolution of neoteny in <i>Ambystoma</i>
title_sort	The neoteny goldilocks zone: The evolution of neoteny in <i>Ambystoma</i>
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author_id_fullname_str_mv	d6cc03a9dd7ef442d82d66f114c9ae58_*_Thomas Lyons d1775d20b12e430869cc7be5d7d4a27e_*_Kevin Arbuckle
author	Thomas Lyons Kevin Arbuckle
author2	Thomas Lyons Kevin Arbuckle
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container_volume	14
container_issue	4
publishDate	2024
institution	Swansea University
issn	2045-7758 2045-7758
doi_str_mv	10.1002/ece3.11240
publisher	Wiley
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description	Neoteny is a developmental strategy wherein an organism reaches sexual maturity without associated adult characteristics. In salamanders, neoteny takes the form of individuals retaining aquatic larval characteristics such as external gills upon maturation. Mole salamanders (Ambystoma) occupy a wide range of habitats and areas across the North American continent, and display examples of non-neotenic, facultatively neotenic and obligate neotenic species, providing high variation for investigating the factors influencing the evolution of neoteny. Here, we use phylogenetic comparative methods to test existing hypotheses that neoteny is associated with elevational and latitudinal distribution, cave-associated isolation, and hybridisation-related polyploidy. We also test if neoteny influences the diversity of habitats a species can occupy, since the restriction to an aquatic life should constrain the availability of different niches. We find that neoteny tends to occur in a narrow latitudinal band between 20–30° North, with particularly narrow latitudinal ranges for obligate compared to facultative neotenic species (16–52° North). We also find that facultatively neotenic species occur at elevations more than twice as high as other species on average, and that species with a higher frequency of neoteny typically have lower habitat diversity. Our results suggest that evolutionary transitions between non-neotenic and facultative neoteny states occur at relatively high and approximately equal rates. Moreover, we estimate that obligate neoteny cannot evolve directly from non-neotenic species (and vice versa), such that facultative neoteny acts as an evolutionary ‘stepping stone’ to and from obligate neoteny. However, our transition rate estimates suggest that obligate neoteny is lost >4-times faster than it evolves, partly explaining the rarity of obligate species. These results support the hypothesis that low latitudes favour the evolution of neoteny, presumably linked to more stable (aquatic) environments due to reduced seasonality, but once evolved it may constrain the diversity of habitats.
published_date	2024-04-08T11:59:54Z
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The neoteny goldilocks zone: The evolution of neoteny in <i>Ambystoma</i>

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