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Article
Exceptional parallelisms characterize the evolutionary transition to live birth in phrynosomatid lizards
Saúl Domínguez-Guerrero
Yale University
Corresponding Author
ORCiD: https://orcid.org/0000-0001-5323-6752
License:
This work is licensed under a CC BY 4.0 License. Read Full License
Viviparity is an evolutionary innovation that enhances maternal protection of developing embryos relative to egg-laying ancestors. The behavioral, physiological, morphological, and life history pathways underpinning this innovation, however, remain unclear. We capitalized on the repeated origin of viviparity in phrynosomatid lizards to tease apart the phenotypic patterns associated with evolutionary transitions to live birth. We detected tandem reductions in mass-specific metabolic rate and mass-specific production in viviparous lineages, in turn reflecting decreases in thermal physiology and fecundity, respectively. These pathways reduce the energetic burden of viviparity without concomitant reductions in offspring body size. Although viviparous lizards are more prevalent in cold environments, transitions in thermal habitat only weakly predict parity mode evolution. Likewise, only cold tolerance adapts rapidly to thermal environment. Heat tolerance and preferred body temperatures track the thermal environment, but with a lag at million-year timescales. This lag likely reflects behavioral buffering: viviparous lizards thermoregulate to low body temperatures, regardless of ambient conditions. Rather than representing an adaptation to cold climates, the lower thermal and metabolic physiology of viviparous species are likely an energetic adjustment for reproduction that facilitated their prolific colonization of cooler environments.
Keywords
viviparity, viviparous lizards, evolutionary transition, live birth
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Due to technical limitations, full-text HTML conversion of this manuscript could not be completed. However, the manuscript can be downloaded and accessed as a PDF.
This is a list of supplementary files associated with this preprint. Click to download.
- SupplementaryInformation.docx
Supplementary_Information
- SupplementaryData1.xlsx
Supplementary_Data_1
- SupplementaryData2.xlsx
Supplementary_Data_2
- PhrynosomatidaeGeneMatrix.txt
Phrynosomatidae_Gene_Matrix
- PhrynosomatidaeTree.txt
Phrynosomatidae_Tree
- Phrynosomatidae500Trees.txt
Phrynosomatidae_500_Trees
- RS.pdf
Reporting Summary
James Van Dyke
ORCiDcommented on 22 January, 2021
This is a really interesting paper, and I was glad to see it come across my google alerts this morning. It is well-written, and the results and conclusions flow clearly from the methods. However, I have a number of concerns about the methods and some of the interpretation. In particular, the way metabolic rate seems to be modelled means that the analysis of metabolic rate variables is entirely artificial. This would be fine for a modelling exercise used to develop a hypothesis, but it falls short for a study that is aiming to test hypotheses about the evolution of viviparity. The paper also largely ignores the effects of allometric relationships and the issues these pose for ratio-based comparisons, which means some of the results are likely to be spurious. Finally, I think the standardization for differences in number of annual reproductive bouts between viviparous and oviparous organisms misses the biological reality of how viviparity constrains annual fecundity, given an animal of X body size. Rather than standardize for these differences- using an approach which directly biases the result- I think they should be included as a dependent variable alongside individual clutch/litter size and egg/offspring size. As a result, I appreciate the effort and I think the results could be valid, but I need more convincing. Despite my criticisms I think it is a very worthwhile project, and I have made extensive comments on a PDF I will email to the contact author which I hope are helpful. I wish the authors the best of luck in publishing this work.
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This preprint is under consideration at a Nature Portfolio Journal. A preprint is a preliminary version of a manuscript that has not completed peer review at a journal. Research Square does not conduct peer review prior to posting preprints. The posting of a preprint on this server should not be interpreted as an endorsement of its validity or suitability for dissemination as established information or for guiding clinical practice.
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Article
Exceptional parallelisms characterize the evolutionary transition to live birth in phrynosomatid lizards
Saúl Domínguez-Guerrero
Yale University
Corresponding Author
ORCiD: https://orcid.org/0000-0001-5323-6752
Badges
Prescreen
This manuscript passed our Prescreen assessment
Complete author information
Appropriate declaration statements
Potential risks to human health
Prescreen
Peer Review Timeline
CURRENT STATUS: Under Review
Version 1
Posted 12 Jan, 2021
Metrics
Comments: 1
PDF Downloads: ...
HTML Views: ...
License:
This work is licensed under a CC BY 4.0 License. Read Full License
Viviparity is an evolutionary innovation that enhances maternal protection of developing embryos relative to egg-laying ancestors. The behavioral, physiological, morphological, and life history pathways underpinning this innovation, however, remain unclear. We capitalized on the repeated origin of viviparity in phrynosomatid lizards to tease apart the phenotypic patterns associated with evolutionary transitions to live birth. We detected tandem reductions in mass-specific metabolic rate and mass-specific production in viviparous lineages, in turn reflecting decreases in thermal physiology and fecundity, respectively. These pathways reduce the energetic burden of viviparity without concomitant reductions in offspring body size. Although viviparous lizards are more prevalent in cold environments, transitions in thermal habitat only weakly predict parity mode evolution. Likewise, only cold tolerance adapts rapidly to thermal environment. Heat tolerance and preferred body temperatures track the thermal environment, but with a lag at million-year timescales. This lag likely reflects behavioral buffering: viviparous lizards thermoregulate to low body temperatures, regardless of ambient conditions. Rather than representing an adaptation to cold climates, the lower thermal and metabolic physiology of viviparous species are likely an energetic adjustment for reproduction that facilitated their prolific colonization of cooler environments.
Figure 1
Figure 2
Figure 3
Due to technical limitations, full-text HTML conversion of this manuscript could not be completed. However, the manuscript can be downloaded and accessed as a PDF.
James Van Dyke
ORCiDcommented on 22 January, 2021
This is a really interesting paper, and I was glad to see it come across my google alerts this morning. It is well-written, and the results and conclusions flow clearly from the methods. However, I have a number of concerns about the methods and some of the interpretation. In particular, the way metabolic rate seems to be modelled means that the analysis of metabolic rate variables is entirely artificial. This would be fine for a modelling exercise used to develop a hypothesis, but it falls short for a study that is aiming to test hypotheses about the evolution of viviparity. The paper also largely ignores the effects of allometric relationships and the issues these pose for ratio-based comparisons, which means some of the results are likely to be spurious. Finally, I think the standardization for differences in number of annual reproductive bouts between viviparous and oviparous organisms misses the biological reality of how viviparity constrains annual fecundity, given an animal of X body size. Rather than standardize for these differences- using an approach which directly biases the result- I think they should be included as a dependent variable alongside individual clutch/litter size and egg/offspring size. As a result, I appreciate the effort and I think the results could be valid, but I need more convincing. Despite my criticisms I think it is a very worthwhile project, and I have made extensive comments on a PDF I will email to the contact author which I hope are helpful. I wish the authors the best of luck in publishing this work.