Evidence for complex life cycle constraints on salamander body form diversification

Bonett, Ronald M.; Blair, Andrea L.

doi:10.1073/pnas.1703877114

Cited by 72 publications

(174 citation statements)

References 81 publications

(121 reference statements)

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“…For the head shape, high within group variance and increased disparity were found at the metamorphosed stage, whereas the body shape was more canalized and conserved. As noted before, during metamorphosis some morphological structures are transformed, whereas other remain relatively unchanged or highly integrated across stages (Bonett and Blair 2017;Bonett et al 2018). Body form and head shape in salamanders can be characterized as traits that undergo a different amount of changes during metamorphosis.…”

Section: Constraint?mentioning

confidence: 78%

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Testing the evolutionary constraints of metamorphosis: The ontogeny of head shape inTriturusnewts

et al. 2019

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In vertebrates with complex, biphasic, life cycles, larvae have a distinct morphology and ecological preferences compared to metamorphosed juveniles and adults. In amphibians, abrupt and rapid metamorphic changes transform aquatic larvae to terrestrial juveniles. The main aim of this study is to test whether, relative to larval stages, metamorphosis (1) resets the pattern of variation between ontogenetic stages and species, (2) constrains intraspecific morphological variability, and (3) similar to the “hour‐glass” model reduces morphological disparity. We explore postembryonic ontogenetic trajectories of head shape (from hatching to completed metamorphosis) of two well‐defined, morphologically distinct Triturus newts species and their F1 hybrids. Variation in head shape is quantified and compared on two levels: dynamic (across ontogenetic stages) and static (at a particular stage). Our results show that the ontogenetic trajectories diverge early during development and continue to diverge throughout larval stages and metamorphosis. The high within‐group variance and the largest disparity level (between‐group variance) characterize the metamorphosed stage. Hence, our results indicate that metamorphosis does not canalize head shape variation generated during larval development and that metamorphosed phenotype is not more constrained relative to larval ones. Therefore, metamorphosis cannot be regarded as a developmental constraint, at least not for salamander head shape.

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Section: Constraint?mentioning

confidence: 78%

“…Starting from previous assumptions, Bonett and Blair (2017) pointed out that some morphological structures could remain relatively unchanged or highly integrated across stages. In such traits, conflicts between structural requirements for carrying out different ecologically relevant functions could limit evolution.…”

mentioning

confidence: 99%

Testing the evolutionary constraints of metamorphosis: The ontogeny of head shape inTriturusnewts

et al. 2019

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“…In performing a similar test of disparity on the species’ mean climates across regions, we observed a much broader range of climatic variation occupied by tropical species (Disp Trop = 7.118, Disp Temp = 3.327, P = 0.001), mirroring the patterns in SA:V evolution. We subsequently constructed a “phyloclimatespace” using phylomorphospace plotting methods and the pruned Bonett and Blair consensus tree (), illustrating that the greater climatic disparity exhibited by tropical species distributions as well as a clear delineation between the temperate and tropical species climates (Fig. 3A) such that there is no overlap of temperate and tropical species’ climatic summaries.…”

Section: Resultsmentioning

confidence: 99%

“…; Blankers et al. ; Baken and Adams , but see Bonett and Blair ). The uniquely compelling results of our study suggest that SA:V may represent a key morphological trait that does respond predictably to environmental selective pressures, as much of the physiology of plethodontids, and thus their organismal performance, is mitigated through the consequences of cutaneous respiration and possible desiccation risk (see Feder ).…”

Section: Discussionmentioning

confidence: 99%

Macroevolution of desiccation‐related morphology in plethodontid salamanders as inferred from a novel surface area to volume ratio estimation approach

2020

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Evolutionary biologists have long been interested in the macroevolutionary consequences of various selection pressures, yet physiological responses to selection across deep time are not well understood. In this paper, we investigate how a physiologically relevant morphological trait, surface area to volume ratio (SA:V) of lungless salamanders, has evolved across broad regional and climatic variation. SA:V directly impacts an organisms’ ability to retain water, leading to the expectation that smaller SA:Vs would be advantageous in arid, water‐limited environments. To explore the macroevolutionary patterns of SA:V, we first develop an accurate method for estimating SA:V from linear measurements. Next, we investigate the macroevolutionary patterns of SA:V across 257 salamander species, revealing that higher SA:Vs phylogenetically correlate with warmer, wetter climates. We also observe higher SA:V disparity and rate of evolution in tropical species, mirrored by higher climatic disparity in available and occupied tropical habitats. Taken together, these results suggest that the tropics have provided a wider range of warmer, wetter climates for salamanders to exploit, thereby relaxing desiccation pressures on SA:V. Overall, this paper provides an accurate, efficient method for quantifying salamander SA:V, allowing us to demonstrate the power of physiological selection pressures in influencing the macroevolution of morphology.

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“…1). This is important in the adaptation and evolution of species (Gould 1977, Deno€ el et al 2005b, Bonett and Blair 2017. Whereas it is obligate in some species that lose the ability to metamorphose, it is a polyphenism in other species (facultative paedomorphosis) and, thus, involves the coexistence of both a paedomorphic and a metamorphic phenotype as a response to environmental drivers (Oromi et al 2016, Mathiron et al 2017).…”

Section: Introductionmentioning

confidence: 99%

Traditionally managed landscapes do not prevent amphibian decline and the extinction of paedomorphosis

Denoël

Ficetola

Sillero

et al. 2019

Ecological Monographs

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Eco‐cultural landscapes are assumed to be favorable environments for the persistence of biodiversity, but global change may affect differently their terrestrial and aquatic components. Few long‐term studies have examined how multiple, global change stressors may affect wetland biodiversity in such environments. Facultative paedomorphosis is a spectacular example of intra‐specific variation, in which biphasic (metamorphosing) amphibians coexist with fully aquatic conspecifics that do not metamorphose (paedomorphs). Paedomorphosis is seriously threatened by global change stressors, but it is unknown to what extent traditional management will allow its long‐term persistence. Here, we tested the effects of alien species introductions while taking into account land use and climate changes on the distribution of two polymorphic newt species (Ichthyosaura alpestris and Lissotriton graecus) in Montenegro by using a 68‐yr data set and Bayesian mixed models integrating complex spatial and temporal structures. We found that, despite the persistence of natural landscapes, metamorphs dramatically declined and paedomorphs were nearly extirpated, losing 99.9% of their aquatic area of occupancy and all the major populations. Fish introduction was the main determinant of decline for both phenotypes. Climate and the presence of crayfish further contributed to the decline of metamorphs, which started later and was less dramatic than that of paedomorphs. The near extinction of paedomorphosis on a country‐wide scale shows how invasive species determine broad‐scale impacts, which can be even stronger than other global change stressors, and underlines the need for immediate management actions to avoid the extinction of a unique developmental process, paedomorphosis.

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Evidence for complex life cycle constraints on salamander body form diversification

Cited by 72 publications

References 81 publications

Testing the evolutionary constraints of metamorphosis: The ontogeny of head shape inTriturusnewts

Testing the evolutionary constraints of metamorphosis: The ontogeny of head shape inTriturusnewts

Macroevolution of desiccation‐related morphology in plethodontid salamanders as inferred from a novel surface area to volume ratio estimation approach

Traditionally managed landscapes do not prevent amphibian decline and the extinction of paedomorphosis

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