Adaptive variation in avian eggshell structure and gas conductance across elevational gradients?
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eLife Assessment
This important study provides evidence, albeit still incomplete, that high-elevation species lose water at slower rates than low-elevation species. The findings imply that egg physiology may be a factor limiting the distributional range of bird species. While this work reinforces the need for all life stages to be considered when evaluating physiological adjustment to climate change, the analyses as presented by the authors do not clearly highlight the specific impact of species differences in influencing these adjustments.
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Abstract
Many tropical species have restricted elevational distributions, which are potentially bounded by constraints imposed by physical conditions on physiological processes. Although some studies have examined variation in the physiology of adult birds with respect to elevation, little attention has been paid to the structure and function of eggshells, which mediate gas exchange between the embryo and the environment. At high elevations, dry air is expected to increase water loss from the egg; selection to avoid desiccation might therefore be expected to favor reduced gas conductance by means of increased eggshell thickness or reduced pore size. We used gas diffusion experiments and scanning electron microscopy to examine water vapor conductance rates and eggshell structures in 197 bird species distributed along an elevational gradient in the Andes. As predicted, water vapor conductance across the eggshell declined in a narrow range with elevation among all species and among species within families, but not among individuals within species. Variation among species in eggshell conductance was lower at high-elevation sites, potentially indicating greater constraints at such sites. Structural changes in eggshells with respect to elevation varied among taxonomic families of birds, suggesting potentially different adaptive responses to common selective pressures in terms of eggshell thickness and pore density, and size. We suggest that considering functional and structural traits of eggshells, which influence embryo development, may help one to better understand the elevational distributions of species and to forecast their responses to global climate change.
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eLife Assessment
This important study provides evidence, albeit still incomplete, that high-elevation species lose water at slower rates than low-elevation species. The findings imply that egg physiology may be a factor limiting the distributional range of bird species. While this work reinforces the need for all life stages to be considered when evaluating physiological adjustment to climate change, the analyses as presented by the authors do not clearly highlight the specific impact of species differences in influencing these adjustments.
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Reviewer #1 (Public Review):
The authors tested the hypothesis that at high elevations avian eggs will be adapted to prevent desiccation that might arise from loss of water to surrounding drier air. They used a combination of gas diffusion experiments and scanning electron microscopy to examine water vapour conductance rates and eggshell structure, including thickness, pore size, and pore density among 197 bird species distributed along an elevational gradient in the Andes. While there was a correlation between water vapour conductance and elevation among species, a decrease in water vapour conductance with elevation was not associated with eggshell thickness, pore size, and pore density, suggesting the variation in the structure of the eggshells is unlikely to do with among species differences in water loss along elevational gradients. …
Reviewer #1 (Public Review):
The authors tested the hypothesis that at high elevations avian eggs will be adapted to prevent desiccation that might arise from loss of water to surrounding drier air. They used a combination of gas diffusion experiments and scanning electron microscopy to examine water vapour conductance rates and eggshell structure, including thickness, pore size, and pore density among 197 bird species distributed along an elevational gradient in the Andes. While there was a correlation between water vapour conductance and elevation among species, a decrease in water vapour conductance with elevation was not associated with eggshell thickness, pore size, and pore density, suggesting the variation in the structure of the eggshells is unlikely to do with among species differences in water loss along elevational gradients. This study is very interesting and timely, especially with increasing water vapour pressure due to climate warming. It is a very well-written study and easy to read. However, I have some concerns about the conclusions drawn from the results.
There are more than twice as many species in low and medium-elevation sites compared to high-elevation sites, so the amount of variation in low and medium-elevation should be expected to be higher by default. The argument for a wider range of variation in low-elevation species will be stronger if the comparison was a similar sample size. Moreover, the pattern clearly breaks down within families. Note also that for Low and medium elevation there is no difference in the amount of variation in conductance residuals possibly because the sample sizes are similar. The seemingly strong positive correlation between eggshell conductance and egg mass may be driven by the five high and two medium-elevation species with large eggs. There seem to be hardly any high-elevation species with egg mass greater than 12g whereas species in low elevation egg size seem to be as high as 80g (Figure 2a). Since larger eggs (and thus eggs of larger birds) lose more water compared to smaller eggs, the correlation between water vapour conductance and elevation may be more strongly associated with body size distribution along elevational gradients rather than egg structure and function.
Authors argue that the observed variation in the relationship between water vapour conductance and elevation among and within bird families suggests potential differences in the adaptive response to common selective pressures in terms of eggshell thickness and pore density, and size. The evidence for this is generally weak from the data analyses because the decrease in water vapour conductance with elevation was not consistent across taxonomic groups nor were differences associated with specific patterns in eggshell thickness and pore density, and size.
It is not clear how the authors expected the relationship between water vapour conductance and elevation to differ among taxonomic groups and there was no attempt to explain the biological implication of these differences among taxonomic groups based on the specific traits of the species or their families. This missing piece of information is crucial to justify the argument that differences among taxonomic groups may be due to differences in adaptive response.
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Reviewer #2 (Public Review):
Many tropical montane species live only within narrow elevational ranges. Rapid climate change has led to considerable interest in determining whether these narrow elevational ranges are the result of physiological specialization: if so, then warming temperatures will have direct fitness consequences. Thus far, studies of tropical montane ectotherms have often found patterns consistent with physiological specialization, while the few field studies of tropical montane birds (endotherms) have not. However, these few studies measured the thermal physiology of adult birds. The early life stages of birds may show physiological specialization, as eggs and nestlings function as ectotherms.
In this paper, Ocampo and colleagues provide the first test of the hypothesis that bird eggs are physiologically specialized to …
Reviewer #2 (Public Review):
Many tropical montane species live only within narrow elevational ranges. Rapid climate change has led to considerable interest in determining whether these narrow elevational ranges are the result of physiological specialization: if so, then warming temperatures will have direct fitness consequences. Thus far, studies of tropical montane ectotherms have often found patterns consistent with physiological specialization, while the few field studies of tropical montane birds (endotherms) have not. However, these few studies measured the thermal physiology of adult birds. The early life stages of birds may show physiological specialization, as eggs and nestlings function as ectotherms.
In this paper, Ocampo and colleagues provide the first test of the hypothesis that bird eggs are physiologically specialized to the climatic conditions of certain elevational zones. They use experiments and observations to measure water vapor conductance rates and eggshell traits in a diverse set of 197 species that live from the lowland Amazon to the high Andes. Ocampo and colleagues present two principal results: (1) High-elevation eggs lose less water over time than do low-elevation eggs, high elevations tend to be less humid than low elevations and (2) Eggshell traits do not show consistent patterns along the elevational gradient. The pattern in water loss is consistent with the hypothesis that high-elevation eggs are physiologically specialized for the slightly drier environments they experience. The finding that eggshell traits did not vary with elevation, however, means that the pattern of water loss is not driven by single eggshell traits (thicker eggshells could reduce water loss rates, as could fewer or smaller eggshell pores).
This paper represents a strong advance for two main reasons. First, it provides evidence that egg physiology varies with elevation as predicted by the hypothesis that eggs are physiologically adapted to certain climatic conditions. This means egg physiological adaptation is a factor that could influence species' elevational ranges. Second, it is a proof-of-concept study that shows it is possible to measure eggshell physiology for a large number of species in the field in order to test hypotheses. As such, it should inspire many further tests that examine adaptation in egg physiology in the context of species' distributions along environmental gradients.
There are two caveats that readers should be aware of. First, measuring these traits is difficult, and there remain questions about the efficacy of different methods. For example, the authors note that quantifying eggshell structures is very difficult, with several unresolved questions about their method of using scanning electron microscopy images to measure eggshell pores. Similarly, the authors mention that temperature variation may partially influence their main result that high-elevation eggs lose water at slower rates than low-elevation eggs (temperatures were colder for experiments at high elevations than for low elevations). Second, I regard the analyses of eggshell traits for specific families as exploratory. There are no a priori expectations for how different families might be expected to differ in their patterns. These analyses are fruitful in that they generate additional hypotheses that future work can test. However, it does mean that the statistical significance of eggshell trait relationships with elevation for specific families should be interpreted with caution.
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Author response:
Reviewer #1 (Public Review):
The authors tested the hypothesis that at high elevations avian eggs will be adapted to prevent desiccation that might arise from loss of water to surrounding drier air. They used a combination of gas diffusion experiments and scanning electron microscopy to examine water vapour conductance rates and eggshell structure, including thickness, pore size, and pore density among 197 bird species distributed along an elevational gradient in the Andes. While there was a correlation between water vapour conductance and elevation among species, a decrease in water vapour conductance with elevation was not associated with eggshell thickness, pore size, and pore density, suggesting the variation in the structure of the eggshells is unlikely to do with among species differences in water loss along …
Author response:
Reviewer #1 (Public Review):
The authors tested the hypothesis that at high elevations avian eggs will be adapted to prevent desiccation that might arise from loss of water to surrounding drier air. They used a combination of gas diffusion experiments and scanning electron microscopy to examine water vapour conductance rates and eggshell structure, including thickness, pore size, and pore density among 197 bird species distributed along an elevational gradient in the Andes. While there was a correlation between water vapour conductance and elevation among species, a decrease in water vapour conductance with elevation was not associated with eggshell thickness, pore size, and pore density, suggesting the variation in the structure of the eggshells is unlikely to do with among species differences in water loss along elevational gradients. This study is very interesting and timely, especially with increasing water vapour pressure due to climate warming. It is a very well-written study and easy to read. However, I have some concerns about the conclusions drawn from the results.
There are more than twice as many species in low and medium-elevation sites compared to high-elevation sites, so the amount of variation in low and medium-elevation should be expected to be higher by default. The argument for a wider range of variation in lowelevation species will be stronger if the comparison was a similar sample size. Moreover, the pattern clearly breaks down within families. Note also that for Low and medium elevation there is no difference in the amount of variation in conductance residuals possibly because the sample sizes are similar. The seemingly strong positive correlation between eggshell conductance and egg mass may be driven by the five high and two medium-elevation species with large eggs. There seem to be hardly any high-elevation species with egg mass greater than 12g whereas species in low elevation egg size seem to be as high as 80g (Figure 2a). Since larger eggs (and thus eggs of larger birds) lose more water compared to smaller eggs, the correlation between water vapour conductance and elevation may be more strongly associated with body size distribution along elevational gradients rather than egg structure and function.
We thank the reviewer for this thoughtful observation. As noted in our response to comment 3, we recognize that the higher number of species at low and mid-elevations reflects the natural turnover in species richness along elevational gradients, and we are transparent about this caveat in our revised Discussion section. Nevertheless, to address this specific concern, we conducted additional analyses excluding the species with large eggs (i.e., egg mass >12g, which are only present at low and mid-elevations in our dataset). These analyses are now included in the Supplementary Figure 1, and the main pattern of lower water vapor conductance at high elevations holds even when larger eggs are excluded.
We agree that the well-known scaling relationship between egg mass and conductance (recognized since the 1970s) may partially explain the observed trends across the elevational gradient. Our aim was to explore whether the known relationship between egg size and conductance varies when incorporating environmental variables such as elevation, which brings with it changes in humidity and oxygen availability. While we acknowledge the possible confounding effect of body size distributions along the gradient, our results, even after controlling for egg size (residual analysis), still suggest a decrease in conductance at higher elevations, consistent with predictions based on environmental conditions.
We have clarified these points in the revised Discussion, including the acknowledgment that disentangling the relative contributions of body size and elevation to conductance patterns remains challenging and warrants further study.
Authors argue that the observed variation in the relationship between water vapour conductance and elevation among and within bird families suggests potential differences in the adaptive response to common selective pressures in terms of eggshell thickness and pore density, and size. The evidence for this is generally weak from the data analyses because the decrease in water vapour conductance with elevation was not consistent across taxonomic groups nor were differences associated with specific patterns in eggshell thickness and pore density, and size.
We appreciate the reviewer’s comments on the observed variation in water vapor conductance across taxonomic groups. As mentioned in response to comment 7, we have removed the explicit analyses and figures showing within-family comparisons, as these were exploratory and not directly tied to a specific hypothesis. We have also toned down our speculations regarding the potential adaptive drivers of the observed variation. In the revised Discussion, we emphasize the need for further research to explore these patterns and acknowledge the limitations of our current dataset in making strong conclusions about the adaptive responses to selective pressures.
It is not clear how the authors expected the relationship between water vapour conductance and elevation to differ among taxonomic groups and there was no attempt to explain the biological implication of these differences among taxonomic groups based on the specific traits of the species or their families. This missing piece of information is crucial to justify the argument that differences among taxonomic groups may be due to differences in adaptive response.
We appreciate the reviewer’s point. To clarify, we were not expecting the relationship between water vapor conductance and elevation to differ among taxonomic groups. Rather, our primary hypothesis was that water vapor conductance would decrease with elevation due to the drier conditions in highland habitats, and we sought to link this pattern with structural characteristics of the eggshell. The suggestion of potential differences among taxonomic groups arose from the lack of a consistent pattern across families, which prompted us to consider possible adaptive variation. We now address this more clearly in the Discussion section, acknowledging the need for further exploration into the potential selective pressures driving this variation among taxonomic groups.
Reviewer #2 (Public Review):
This paper represents a strong advance for two main reasons. First, it provides evidence that egg physiology varies with elevation as predicted by the hypothesis that eggs are physiologically adapted to certain climatic conditions. This means egg physiological adaptation is a factor that could influence species' elevational ranges. Second, it is a proof-of-concept study that shows it is possible to measure eggshell physiology for a large number of species in the field in order to test hypotheses. As such, it should inspire many further tests that examine adaptation in egg physiology in the context of species' distributions along environmental gradients.
There are two caveats that readers should be aware of. First, measuring these traits is difficult, and there remain questions about the efficacy of different methods. For example, the authors note that quantifying eggshell structures is very difficult, with several unresolved questions about their method of using scanning electron microscopy images to measure eggshell pores. Similarly, the authors mention that temperature variation may partially influence their main result that high-elevation eggs lose water at slower rates than low-elevation eggs (temperatures were colder for experiments at high elevations than for low elevations). Second, I regard the analyses of eggshell traits for specific families as exploratory. There are no a priori expectations for how different families might be expected to differ in their patterns. These analyses are fruitful in that they generate additional hypotheses that future work can test. However, it does mean that the statistical significance of eggshell trait relationships with elevation for specific families should be interpreted with caution.
We thank Reviewer 2 for these insightful comments. As mentioned earlier, measuring these traits is indeed very challenging, and we acknowledge the limitations of our methods, particularly when it comes to using scanning electron microscopy to quantify eggshell structures. We are aware of the unresolved questions around these techniques, and we plan to continue refining these methods in future studies. Regarding the influence of temperature variation on water loss, we recognize that colder temperatures at high elevations may have influenced our results, and we address this potential confounding factor in the Discussion section, Line 257.
We also agree with the reviewer’s point regarding the exploratory nature of the family-specific analyses. These analyses were not guided by specific hypotheses, other than the expectation of replicating the overall pattern, and we recognize that they should be interpreted with caution. They serve primarily to generate additional hypotheses for future studies. In the revised manuscript, we have toned down the emphasis on the statistical significance of eggshell trait relationships with elevation for specific families, and we emphasize the need for further research to confirm these patterns.
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