Response to von Schmalensee et al.

Von Schmalensee et al. present two concerns about our study. While the first stems from a general disagreement about our simulation methodology, the second is a useful observation of a modelling choice we made that affected simulation outcomes, but in ways that do not invalidate our original conclusions.

3D printed models are an accurate, cost-effective, and reproducible tool for quantifying terrestrial thermal environments.

Predicting ecological responses to rapid environmental change has become one of the greatest challenges of modern biology. One of the major hurdles in forecasting these responses is accurately quantifying the thermal environments that organisms experience. The distribution of temperatures available within an organism's habitat is typically measured using data loggers called operative temperature models (OTMs) that are designed to mimic certain properties of heat exchange in the focal organism. The gold standard for OTM construction in studies of terrestrial ectotherms has been the use of copper electroforming which creates anatomically accurate models that equilibrate quickly to ambient thermal conditions. However, electroformed models require the use of caustic chemicals, are often brittle, and their production is expensive and time intensive. This has resulted in many researchers resorting to the use of simplified OTMs that can yield substantial measurement errors. 3D printing offers the prospect of robust, easily replicated, morphologically accurate, and cost-effective OTMs that capture the benefits but alleviate the problems associated with electroforming. Here, we validate the use of OTMs that were 3D printed using several materials across eight lizard species of different body sizes and living in habitats ranging from deserts to tropical forests. We show that 3D printed OTMs have low thermal inertia and predict the live animal's equilibration temperature with high accuracy across a wide range of body sizes and microhabitats. Finally, we developed a free online repository and database of 3D scans (https://www.3dotm.org/) to increase the accessibility of this tool to researchers around the world and facilitate ease of production of 3D printed models. 3D printing of OTMs is generalizable to taxa beyond lizards. If widely adopted, this approach promises greater accuracy and reproducibility in studies of terrestrial thermal ecology and should lead to improved forecasts of the biological impacts of climate change.

Evolutionary constraints mediate extinction risk under climate change.

Mounting evidence suggests that rapid evolutionary adaptation may rescue some organisms from the impacts of climate change. However, evolutionary constraints might hinder this process, especially when different aspects of environmental change generate antagonistic selection on genetically correlated traits. Here, we use individual-based simulations to explore how genetic correlations underlying the thermal physiology of ectotherms might influence their responses to the two major components of climate change-increases in mean temperature and thermal variability. We found that genetic correlations can influence population dynamics under climate change, with declines in population size varying three-fold depending on the type of correlation present. Surprisingly, populations whose thermal performance curves were constrained by genetic correlations often declined less rapidly than unconstrained populations. Our results suggest that accurate forecasts of the impact of climate change on ectotherms will require an understanding of the genetic architecture of the traits under selection.

Realistic genetic architecture enables organismal adaptation as predicted under the folk definition of inclusive fitness.

A fundamental task of evolutionary biology is to explain the pervasive impression of organismal design in nature, including traits benefiting kin. Inclusive fitness is considered by many to be a crucial piece in this puzzle, despite ongoing discussion about its scope and limitations. Here, we use individual-based simulations to study what quantity (if any) individual organisms become adapted to maximize when genetic architectures are more or less suitable for the presumed main driver of biological adaptation, namely cumulative multi-locus evolution. As an expository device, we focus on a hypothetical situation called Charlesworth's paradox, in which altruism is seemingly predicted to evolve, yet altruists immediately perish along with their altruistic genes. Our results support a recently proposed re-definition of inclusive fitness, which is concerned with the adaptive design of whole organisms as shaped by multi-locus evolution, rather than with selection for any focal gene. They also illustrate how our conceptual understanding of adaptation at the phenotypic level should inform our choice of genetic assumptions in abstract simplified models.

Visible implant elastomer (VIE) success in early larval stages of a tropical amphibian species.

Animals are often difficult to distinguish at an individual level, and being able to identify individuals can be crucial in ecological or behavioral studies. In response to this challenge, biologists have developed a range of marking (tattoos, brands, toe-clips) and tagging (banding, collars, PIT, VIA, VIE) methods to identify individuals and cohorts. Animals with complex life cycles are notoriously hard to mark because of the distortion or loss of the tag across metamorphosis. In amphibians, few studies have attempted larval tagging and none have been conducted on a tropical species. Here, we present the first successful account of VIE tagging in early larval stages (Gosner stage 25) of the dyeing poison frog (Dendrobates tinctorius) coupled with a novel anesthetic (2-PHE) application for tadpoles that does not require buffering. Mean weight of individuals at time of tagging was 0.12 g, which is the smallest and developmentally youngest anuran larvae tagged to date. We report 81% tag detection over the first month of development, as well as the persistence of tags across metamorphosis in this species. Cumulative tag retention vs tag observation differed by approximately 15% across larval development demonstrating that "lost" tags can be found later in development. Tagging had no effect on tadpole growth rate or survival. Successful application of VIE tags on D. tinctorius tadpoles introduces a new method that can be applied to better understand early life development and dispersal in various tropical species.