Exceptional parallelisms characterize the evolutionary transition to live birth in phrynosomatid lizards
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.
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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.
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Supplementary_Information
Supplementary_Data_1
Supplementary_Data_2
Phrynosomatidae_Gene_Matrix
Phrynosomatidae_Tree
Phrynosomatidae_500_Trees
Reporting Summary
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.
Posted 12 Jan, 2021
Exceptional parallelisms characterize the evolutionary transition to live birth in phrynosomatid lizards
Posted 12 Jan, 2021
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.
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.