Dynamics of body mass and oxygen consumption in the ontogeny of the Spanish ribbed newt (Pleurodeles waltl): 2. Larval stage

Vladimirova, I. G.; Kleimenov, S. Yu.; Алексеева, Т. А.

doi:10.1134/s106235901201013x

Cited by 5 publications

(6 citation statements)

References 14 publications

(33 reference statements)

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“…Once abrupt metamorphosis begins, feeding ceases, although there are mixed anecdotal reports of transforming organisms feeding or attempting to feed in the lab ( Deban and Marks 2002 ). Metamorphosis itself does not increase energetic demand, as evidenced by gradually metamorphosing salamanders, in which metabolic rate remains unchanged during the transformation ( Vladimirova et al 2012 ). However, the transformation is more extensive in abrupt metamorphosing salamanders, and frogs experience elevated metabolic rates during their extensive metamorphosis ( Orlofske and Hopkins 2009 ; Wright et al 2011 ).…”

Section: Discussionmentioning

confidence: 99%

Metamorphosis Imposes Variable Constraints on Genome Expansion through Effects on Development

Mueller

Cressler

Schwartz

et al. 2023

Integrative Organismal Biology

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Genome size varies ∼ 100,000-fold across eukaryotes and has long been hypothesized to be influenced by metamorphosis in animals. Transposable element accumulation has been identified as a major driver of increase, but the nature of constraints limiting the size of genomes has remained unclear, even as traits such as cell size and rate of development co-vary strongly with genome size. Salamanders, which possess diverse metamorphic and non-metamorphic life histories, join the lungfish in having the largest vertebrate genomes ࣧ 3 to 40 times that of humans ࣧ as well as the largest range of variation in genome size. We tested 13 biologically-inspired hypotheses exploring how the form of metamorphosis imposes varying constraints on genome expansion in a broadly representative phylogeny containing 118 species of salamanders. We show that metamorphosis during which animals undergo the most extensive and synchronous remodeling imposes the most severe constraint against genome expansion, with the severity of constraint decreasing with reduced extent and synchronicity of remodeling. More generally, our work demonstrates the potential for broader interpretation of phylogenetic comparative analysis in exploring the balance of multiple evolutionary pressures shaping phenotypic evolution.

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Section: Discussionmentioning

confidence: 99%

Metamorphosis Imposes Variable Constraints on Genome Expansion through Effects on Development

Mueller

Cressler

Schwartz

et al. 2023

Integrative Organismal Biology

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“…Despite being homologous and retaining broad similarities at the transcriptomic, hormonal, and organismal levels (Sanchez, et al 2018), salamander metamorphosis is different — and less dramatic — than frog metamorphosis. The process takes much longer in salamanders; timescales are on the order of weeks to months rather than days (Norman 1985; Downie, et al 2004; Vladimirova, et al 2012; Sanchez, et al 2018), suggesting little, if any, time pressure. Metamorphosing salamanders do not experience compromised locomotion and are thus not more vulnerable to predation as are frogs (Landberg and Azizi 2010).…”

Section: Discussionmentioning

confidence: 99%

“…Metamorphosing salamanders do not experience compromised locomotion and are thus not more vulnerable to predation as are frogs (Landberg and Azizi 2010). In addition, metamorphosing salamanders do not have higher energetic requirements compared to non-metamorphosing individuals of the same species (Vladimirova, et al 2012). Some salamanders, however, are unable to feed during metamorphosis, requiring that they undergo the transformation using only stored energy reserves (i.e., non-feeding metamorphosers) (Deban and Marks 2002)).…”

Section: Discussionmentioning

confidence: 99%

“…Once abrupt metamorphosis begins, feeding ceases, although there are mixed anecdotal reports of transforming organisms feeding or attempting to feed in the lab (Deban and Marks 2002). Metamorphosis itself does not increase energetic demand, as evidenced by gradually metamorphosing salamanders, in which metabolic rate remains unchanged during the transformation (Vladimirova, et al 2012). However, the transformation is more extensive in abrupt metamorphosing salamanders, and frogs experience elevated metabolic rates during their extensive meta-morphosis (Orlofske and Hopkins 2009; Wright, et al 2011).…”

Section: Discussionmentioning

confidence: 99%

“…However, the transformation is more extensive in abrupt metamorphosing salamanders, and frogs experience elevated metabolic rates during their extensive meta-morphosis (Orlofske and Hopkins 2009; Wright, et al 2011). Thus, abrupt metamor-phosers are at risk of initiating a costly sequence of developmental events with sub-optimal energy reserves and impaired capacity to feed (Deban and Marks 2002; Vladimirova, et al 2012; Beachy, et al 2017). In contrast, gradual metamorphosers are not affected energetically, as they can feed throughout metamorphosis as well as delay its onset.…”

Section: Discussionmentioning

confidence: 99%

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Metamorphosis imposes variable constraints on genome expansion through effects on development

Cressler²,

et al. 2021

Preprint

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Genome size varies ~ 100,000-fold across eukaryotes. Genome size is heavily shaped by transposable element accumulation, the dynamics of which are increasingly well understood. However, given that traits like cell size and rate of development co-vary strongly with genome size, organism-level trait evolution likely shapes genome size diversity as well. Metamorphosis -- a radical transformation of morphology -- has been hypothesized to impact genome size because it can be a vulnerable part of the life cycle. Thus, selection may act to limit metamorphic duration, indirectly constraining the rate of development as well as genome and cell sizes. Salamanders have large and variable genomes -- 3 to 40 times that of humans -- and species exhibit a range of metamorphic and non-metamorphic life histories. Using salamanders, we test the hypothesis that different types of metamorphic repatterning during the life cycle impose different constraints on genome expansion. We show that metamorphosis during which animals are unable to feed imposes the most severe constraint against genome expansion. Other types of metamorphosis that differ in energetic provisioning impose less severe constraints. More generally, our work demonstrates the utility of phylogenetic comparative methods in testing the role of constraint in shaping phenotypic evolution.

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A comparative analysis testing Werner's theory of complex life cycles

2022

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1. A popular theoretical model for explaining the evolution of complex life cycles (CLCs) was provided by Earl Werner. The theory predicts the size at which an individual should switch stages to maximise growth rate relative to mortality rate across the life history.2. Werner's theory assumes that body size does not change during the transition from one phase to another (e.g. from larva to adult)-a key assumption that has not been tested systematically but could alter the predictions of the model.3. We quantified how growth rate and mass change across larval stages and metamorphosis for 105 species of fish, amphibians, insects, crustaceans and molluscs. Across all taxonomic groups, we found support for Werner's assumption that growth rates are maintained or increase around transitions. We found that changes in growth and mass were greatest during metamorphosis, and change in growth correlated with development time. Importantly, most species either gained or lost mass when switching to a new stage-a direct contradiction of Werner's assumption. When we explored the consequences of energy loss and gain in a numerical model, we found that individuals should switch stages at a larger and smaller size, respectively, relative to what Werner's standard theory predicts. 4. Our results suggest that while there is support for Werner's assumption regarding growth rates, mass changes profoundly alter the timing of transitions that are predicted to maximise fitness, and therefore the original model omits an important component that may contribute to the evolution of CLCs. Future studies should test for conditions that alter the costs of transitions, so that we can have a better understanding of how mass loss or gain affects fitness.

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Dynamics of body mass and oxygen consumption in the ontogeny of the Spanish ribbed newt (Pleurodeles waltl): 2. Larval stage

Cited by 5 publications

References 14 publications

Metamorphosis Imposes Variable Constraints on Genome Expansion through Effects on Development

Metamorphosis Imposes Variable Constraints on Genome Expansion through Effects on Development

Metamorphosis imposes variable constraints on genome expansion through effects on development

A comparative analysis testing Werner's theory of complex life cycles

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