Advancing perspectives on parity‐mode evolution

Pyron, R. Alexander

doi:10.1002/jez.b.22644

Cited by 13 publications

(11 citation statements)

References 20 publications

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“…Phylogenetic reconstruction of the transitions in reproductive mode in squamates is a contentious topic (King and Lee, 2015;Pyron, 2015;Pyron and Burbrink, 2014). Our reanalysis of published data on reproductive mode recovers similar results to King and Lee 2015 (see methods for information on importance of rate shifts in viviparity), but is not intended to add to, or resolve, this controversy, which requires greater phylogenetic resolution and/or data on reproductive mode.…”

Section: Female Behavioural Plasticity Resolves the Constraints Imposed By Thermal Physiologysupporting

confidence: 75%

Maternal behavioural thermoregulation facilitated evolutionary transitions from egg laying to live birth

Pettersen

Feiner

Noble

et al. 2021

Preprint

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Live birth is a key innovation that has evolved from egg laying over 100 times in reptiles. One significant feature in this transition is the thermal conditions experienced by developing embryos. Adult lizards and snakes often have preferred body temperatures that can be lethal to developing embryos and should prevent egg retention: how has viviparity repeatedly evolved in the face of this pervasive mismatch? Here we resolve this paradox by conducting phylogenetic analyses using data on thermal preference from 224 species. Thermal mismatches between mothers and offspring are widespread but resolved by gravid females behaviourally down-regulating their body temperature towards the thermal optimum of embryos. Importantly, this thermoregulatory behaviour evolved in ancestral egg-laying species before the evolutionary emergence of live birth. Maternal thermoregulatory behaviour therefore bypasses constraints imposed by a slowly evolving thermal physiology and is likely to have been a key requirement for repeated transitions to live birth.

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Section: Female Behavioural Plasticity Resolves the Constraints Imposed By Thermal Physiologysupporting

confidence: 75%

Maternal behavioural thermoregulation facilitated evolutionary transitions from egg laying to live birth

Pettersen

Feiner

Noble

et al. 2021

Preprint

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“…To examine the robustness of our predictions to the realistic distribution of squamates, we downloaded species’ distribution shapefiles from the IUCN Red List Spatial Data (http://www.iucnredlist.org/) and a reference table of squamate reproductive modes from the literature (Pyron, ). Then we extracted in R (library ‘raster’) a list of species presented in each 1° × 1° grid cell (in the WGS84 projection; 1° represent 111.32 km at equator) and calculated the percentage of species that were viviparous.…”

Section: Methodsmentioning

confidence: 99%

A global test of the cold‐climate hypothesis for the evolution of viviparity of squamate reptiles

Buckley

Huey

et al. 2018

Global Ecol Biogeogr

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Aim The evolution of viviparity in squamate reptiles has attracted considerable scientific attention since the beginning of last century. The cold‐climate hypothesis posits that cold regions favor viviparity (and therefore the incidence of viviparous squamates is increased in these regions) because viviparous females can use thermoregulatory behavior to shorten embryonic developmental time and to reduce exposure of embryos to stressful temperatures. However, a rigorous global‐scale test of the impact of viviparity on the developmental time and viability of embryos is still absent. Recently developed biophysical models and climate databases enable us to conduct a mechanistic test of this hypothesis. Location Global. Time period Summer. Major taxa studied Squamata. Methods We integrated global climate data, a biophysical model, and developmental functions to quantify the effects of temperature on embryo developmental time, developmental viability, and energy consumption of oviparous versus viviparous embryos. To examine the accuracy of our predictions, we calculated the percentage of squamate reptiles that were viviparous in each region and assessed developmental temperature of gravid females, latitude and elevation as predictors for the percentage of squamate reptiles. Results Compared with oviparous embryos, viviparous embryos develop faster in cold regions, and experience similar embryonic developmental viability. Across most latitudes and elevations, the total energetic cost of development is lower for viviparous embryos than for oviparous embryos. Cold regions contain a higher proportion of viviparous species than do hot regions. By comparing the distribution pattern of viviparity and temperature effects on embryonic development, we found that shortened development time provided the strongest benefit of viviparity. Main conclusions Our global and biophysical model based comparison generally supports the cold‐climate hypothesis. Moreover, viviparity in cold climates appears beneficial primarily by shortening developmental time.

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“…While a recent analysis suggested that the number of independent origins of viviparity may be controversial, there is a consilience of data that counters any suggestion that there have been a high number of reversions from a viviparous to oviparous reproductive mode (Griffith et al 2015; Shine 2015; Wright et al 2015). The presentation of these data led the lead author of the original analyses to concede that the data support the hypothesis that there have been frequent transitions to viviparity in squamates (Pyron 2015). In viviparous squamates, a vast majority of placentae are simple structures with mainly gas and water exchange functions, and the embryo relies on yolk reserves for nutrition, much like an embryo of an oviparous species.…”

Section: Introductionmentioning

confidence: 99%

Reptile Pregnancy Is Underpinned by Complex Changes in Uterine Gene Expression: A Comparative Analysis of the Uterine Transcriptome in Viviparous and Oviparous Lizards

et al. 2016

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The evolution of new organs is difficult to study because most vertebrate organs evolved only once, more than 500 million years ago. An ideal model for understanding complex organ evolution is the placenta, a structure that is present in live bearing reptiles and mammals (amniotes), which has evolved independently more than 115 times. Using transcriptomics, we characterized the uterine gene expression patterns through the reproductive cycle of a viviparous skink lizard, Pseudemoia entrecasteauxii. Then we compare these patterns with the patterns of gene expression from two oviparous skinks Lampropholis guichenoti and Lerista bougainvillii. While thousands of genes are differentially expressed between pregnant and non-pregnant uterine tissue in the viviparous skink, few differentially expressed genes were identified between gravid and non-gravid oviparous skinks. This finding suggests that in P. entrecasteauxii, a pregnant-specific gene expression profile has evolved, allowing for the evolution of pregnancy-specific innovations in the uterus. We find substantial gene expression differences between the uterus of the chorioallantoic and the yolk sac placenta in P. entrecasteauxii, suggesting these placental regions are specialized for different placental functions. In particular, the chorioallantoic placenta is likely a major site of nutrient transport by membrane-bound transport proteins, while the yolk sac placenta also likely transports nutrients but via apocrine secretions. We discuss how the evolution of transcription factor networks is likely to underpin the evolution of the new transcriptional states in the uterine tissue of viviparous reptiles.

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Advancing perspectives on parity‐mode evolution

Cited by 13 publications

References 20 publications

Maternal behavioural thermoregulation facilitated evolutionary transitions from egg laying to live birth

Maternal behavioural thermoregulation facilitated evolutionary transitions from egg laying to live birth

A global test of the cold‐climate hypothesis for the evolution of viviparity of squamate reptiles

Reptile Pregnancy Is Underpinned by Complex Changes in Uterine Gene Expression: A Comparative Analysis of the Uterine Transcriptome in Viviparous and Oviparous Lizards

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