Complex plumages spur rapid color diversification in kingfishers (Aves: Alcedinidae)

  1. Chad M Eliason
  2. Jenna M McCullough
  3. Shannon J Hackett
  4. Michael J Andersen

  • Curated by eLife

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    This important work advances our understanding of the factors that affect the speed of colour evolution in birds and the resulting diversification patterns. It provides compelling evidence that more complex plumage coloration can lead to rapid colour evolution in kingfishers, and could pave the way for more comprehensive analyses that fully embrace the multidimensional nature of colour variation. Hence, the results will be of broad interest to ornithologists and evolutionary biologists in general, once the authors have streamlined the theoretical framework and explained the novel methodological approaches in more detail.

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Abstract

Colorful signals in nature provide some of the most stunning examples of rapid phenotypic evolution. Yet, studying color pattern evolution has been historically difficult owing to differences in perceptual ability of humans and analytical challenges with studying how complex color patterns evolve. Island systems provide a natural laboratory for testing hypotheses about the direction and magnitude of phenotypic change. A recent study found that plumage colors of island species are darker and less complex than continental species. Whether such shifts in plumage complexity are associated with increased rates of color evolution remains unknown. Here, we use geometric morphometric techniques to test the hypothesis that plumage complexity and insularity interact to influence color diversity in a species-rich clade of colorful birds—kingfishers (Aves: Alcedinidae). In particular, we test three predictions: (1) plumage complexity enhances interspecific rates of color evolution, (2) plumage complexity is lower on islands, and (3) rates of plumage color evolution are higher on islands. Our results show that more complex plumages result in more diverse colors among species and that island species have higher rates of color evolution. Importantly, we found that island species did not have more complex plumages than their continental relatives. Thus, complexity may be a key innovation that facilitates evolutionary response of individual color patches to distinct selection pressures on islands, rather than being a direct target of selection itself. This study demonstrates how a truly multivariate treatment of color data can reveal evolutionary patterns that might otherwise go unnoticed.

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  1. Version published to 10.7554/elife.83426 on eLife
  2. eLife

    Author Response

    Reviewer #1 (Public Review):

    Animal colour evolution is hard to study because colour variation is extremely complex. Colours can vary from dark to light, in their level of saturation, in their hue, and on top of that different parts of the body can have different colours as well, as can males and females. The consequence of this is that the colour phenotype of a species is highly dimensional, making statistical analyses challenging.

    Herein the authors explore how colour complexity and island versus mainland dwelling affect the rates of colour evolution in a colourful clade of birds: the kingfishers. Island-dwelling has been shown before to lead to less complex colour patterns and darker coloration in birds across the world, and the authors hypothesise that lower plumage complexity should lead to lower evolutionary rates. In this paper, the authors explore a variety of different and novel statistical approaches in detail to establish the mechanism behind these associations.

    There are three main findings: (1) rates of colour evolution are higher for species that have more complex colour phenotypes (e.g. multiple different colour patches), (2) rates of colour evolution are higher on island kingfishers, but (3) this is not because island kingfishers have a higher level of plumage complexity than their mainland counterparts.

    I think that the application of these multivariate methods to the study of colour evolution and the results could pave the way for new studies on colour evolution.

    We appreciate this positive comment about our manuscript.

    I do, however, have a set of suggestions that should hopefully improve the robustness of results and clarity of the paper as detailed below:

    1. The two main hypotheses tested linking plumage complexity and island-dwelling to rates of colour evolution seem rather disjointed in the introduction. This section should integrate these two aspects better justifying why you are testing them in the same paper. In my opinion, the main topic of the paper is colour evolution, not island-mainland comparisons. I would suggest starting with colours and the challenges associated with the study of colour evolution and then introducing other relevant aspects.

    We implemented this suggestion by reorganizing the introduction to introduce color/and challenges with studying it (para 1), then we discuss plumage complexity (para 2). We follow this with a paragraph about the importance of islands in testing evolutionary hypotheses (para 3), and onto kingfishers as a model system (para 4) and our hypothesis/predictions (para 5).

    1. Title: the title refers to both complex plumage and island-dwelling, but the potential effects of complexity should apply regardless of being an island or mainland-dwelling species, am I right? Consider dropping the reference to islands in the title.

    We removed “island” from the title.

    1. The results encompass a large variety of statistical results some closely related to the main hypothesis (eg island/mainland differences) tested and others that seem more tangential (differences between body parts, sexes). Moreover, quite a few different approaches are used. I think that it would be good to be a bit more selective and concentrate the paper on the main hypotheses, in particular, because many results are not mentioned or discussed again outside the Results section.

    We removed analyses that we felt were distracting from our main point (e.g., MCMCglmm) and streamlined our approach to use PGLS methods for both rates (phylolm) and multivariate color patterns (d-PGLS). The relevance of sex differences in coloration is also made more clear, as we added details about how we tested for a relationship between male and female coloration and that we use this strong correlation as a justification for averaging color by species (e.g., see lines 369-375).

    1. Related to the previous section, the variety of analytical approaches used is a bit bewildering and for the reader, it is unclear why different options were used in different sections. Again, streamlining would be highly desirable, and given the novel nature of the analytical approach (as far as I know, many analytical approaches are applied for the first time to study colour evolution) it would be good to properly explain them to the reader, highlighting their strengths and weaknesses.

    We appreciate the suggestion and have now included a workflow diagram, as suggested (see Figure 1). We further added considerable detail to the Methods (old length = 502 words, new length = 1355 words) and mention caveats of the approaches we have taken (e.g., line 308: “We used photosensitivity data for the blue tit (Hart et al., 2000) due to the limited availability of sensitivity data for other avian species”).

    1. The Results section contains quite a bit of discussion (and methods) despite there being a separate Discussion section. I suggest either separating them better or joining them completely.

    We appreciate this. We were following other eLife articles that include more discussion within the Results, therefore we would prefer to leave these aspects in place. However, we did move a considerable amount of information from the Results section to the Methods section. In addition, we also reorganized the Results to better match the logical flow of the Introduction. The end result, we hope, is a Results section that is considerably more streamlined.

    1. The main analyses of colour evolutionary rates only include chromatic aspects of colour variation. Why was achromatic variation (i.e. light to dark variation) not included in the analyses? I think that such variation is an important part of the perceived colour (e.g. depending on their lightness the same spectral shape could be perceived as yellow or green, black or grey or white). I realize that this omission is not uncommon and I have done so myself in the past, but I think that in this case, it is highly relevant to include it in the analyses (also because previous work suggests that island birds are darker than their mainland counterparts). This should be possible, as achromatic variation may be estimated using double cone quantum catches (Siddiqi et al., 2004) and the appropriate noise-to-signal ratios (Olsson et al., 2018). Adding one extra dimension per plumage patch should not pose substantial computational difficulties, I think.

    We incorporated this suggestion and we have now fully integrated achromatic color variation into all of our analyses. These new analyses let us compare results to previous work showing that island birds are darker than mainland counterparts. We further discuss the caveats of chromatic and achromatic channels (e.g., lines 313-317: “Although it is possible, in theory, to combine chromatic and achromatic channels of color variation in a single analysis (Pike, 2012), we opted to analyze them separately, as these different channels are likely under different selection pressures (Osorio and Vorobyev, 2005).”).

    1. The methods need to be much better explained. Currently, some methods are explained in the main text and some in the methods section. All methods should be explained in detail in the methods section and I suggest that it would be better to use a more traditional manuscript structure with Methods before Results (IMRaD), to avoid repetition (provided this is allowed by the journal). Whenever relevant the authors need to explain the choice of alternative approaches. Many functions used have different arguments that affect the outcome of the analyses, these need to be properly explained and justified. In general, most readers will not check the R script, and the methods should be understandable to readers that are not familiar with R. This is particularly important because I think that the methodological approach used will be one of the main attractions of the manuscript, and other researchers should be able to implement it on their own data with ease. Judging from the R script, there are quite a few analyses that were not reported in the manuscript (e.g. multivariate evolutionary rates being higher in forest species). This should be fixed/clarified.

    We clarified several methodological details in the manuscript (e.g., added package versions throughout, mention the permutation option used for compare.evol.rates, cited RPANDA) and modified the Methods section considerably to make logical connections among the sections. We also checked and cleaned up the R markdown file to ensure the analyses were in sync with the manuscript analyses.

    Reviewer #2 (Public Review):

    In "Complex plumages spur rapid color diversification in island kingfishers (Aves: Alcedinidae)", Eliason et al. link intraspecific plumage complexity with interspecific rates of plumage evolution. They demonstrate a correlation here and link this with the distinction between island and mainland taxa to create a compelling manuscript of general interest on drivers of phenotypic divergence and convergence in different settings.

    This will be a fantastic contribution to the literature on the evolution of plumage color and pattern and to our understanding of phenotypic divergence between mainland and island taxa. A few key revisions can help it get there. This paper needs to get, fairly quickly, up to a point where the difference between plumage complexity and color divergence is defined carefully. That should include hammering home that one is an intraspecific measure, while one is an interspecific measure. It took me three reads of the paper to be able to say this with confidence. Leading with that point will greatly improve the paper if that point gets forgotten then the premise of the paper feels very circular.

    We hope our considerable modifications throughout–including explicitly mentioning that complexity is an intraspecific measure whereas rates are interspecific (e.g., see lines 65, 140, 170, 667)–have made the premise of the paper more clear. We also added a new workflow figure (Figure 1) that includes example species pairs showing cases in which intraspecific plumage complexity and interspecific color divergence could show a negative relationship, rather than a positive one as we predict in the manuscript. We discuss this detail in lines 159-161 (“However, this is not necessarily the case, as there are examples within kingfishers that show simple plumages yet high color divergence, as well as complex plumages with little evolutionary divergence (Figure 1B).”).

    Also importantly, somewhere early on a hypothesized causal pathway by which insularity, plumage complexity, and color divergence interact needs to be laid out. The analyses that currently follow are good ones, and not wrong, but it's challenging to assess whether they are the right ones to run because I'm not following the authors' reasoning very well here. I think it's possible a more holistic analysis could be done here, but I'll refrain from any such suggestions until I better get what the authors are trying to link.

    We overhauled the Introduction. This included adding lines that connect the ideas of complexity and insularity (lines 65-58: “intraspecific plumage complexity (i.e., the degree of variably colored patches across a bird's body) could be a key innovation that drives rates of color evolution in birds and should be considered alongside ecological and geographic hypotheses.”) and insularity and color divergence (lines 69-85). We also rethought the analyses and now include PGLS analyses using tip-based rates that allow us to account for both insularity and complexity in the same analysis.

    We also need something near the top that tells us a bit more about the biogeography of kingfishers. Are kingfisher species always allopatric? I know the answer is no, but not all readers will. What I know less well though is whether your insular species are usually allopatric. I suspect the answer is yes, but I don't actually know.

    Great point. We have added details to the manuscript to clarify this (e.g., line 214: “The number of sympatric lineages ranged from 1–9 on islands, and 6–38 for mainland taxa.”).

    In short, how do the authors think allopatry/sympatry/opportunity for competition link to mainland vs. island link to plumage complexity? And rates of color evolution? Make this clear upfront.

    We believe our revised introduction makes these connections much clearer.

  3. eLife

    eLife assessment

    This important work advances our understanding of the factors that affect the speed of colour evolution in birds and the resulting diversification patterns. It provides compelling evidence that more complex plumage coloration can lead to rapid colour evolution in kingfishers, and could pave the way for more comprehensive analyses that fully embrace the multidimensional nature of colour variation. Hence, the results will be of broad interest to ornithologists and evolutionary biologists in general, once the authors have streamlined the theoretical framework and explained the novel methodological approaches in more detail.

  4. eLife

    Reviewer #1 (Public Review):

    Animal colour evolution is hard to study because colour variation is extremely complex. Colours can vary from dark to light, in their level of saturation, in their hue, and on top of that different parts of the body can have different colours as well, as can males and females. The consequence of this is that the colour phenotype of a species is highly dimensional, making statistical analyses challenging.

    Herein the authors explore how colour complexity and island versus mainland dwelling affect the rates of colour evolution in a colourful clade of birds: the kingfishers. Island-dwelling has been shown before to lead to less complex colour patterns and darker coloration in birds across the world, and the authors hypothesise that lower plumage complexity should lead to lower evolutionary rates. In this paper, the authors explore a variety of different and novel statistical approaches in detail to establish the mechanism behind these associations.

    There are three main findings: (1) rates of colour evolution are higher for species that have more complex colour phenotypes (e.g. multiple different colour patches), (2) rates of colour evolution are higher on island kingfishers, but (3) this is not because island kingfishers have a higher level of plumage complexity than their mainland counterparts.

    I think that the application of these multivariate methods to the study of colour evolution and the results could pave the way for new studies on colour evolution.

    I do, however, have a set of suggestions that should hopefully improve the robustness of results and clarity of the paper as detailed below:

    1. The two main hypotheses tested linking plumage complexity and island-dwelling to rates of colour evolution seem rather disjointed in the introduction. This section should integrate these two aspects better justifying why you are testing them in the same paper. In my opinion, the main topic of the paper is colour evolution, not island-mainland comparisons. I would suggest starting with colours and the challenges associated with the study of colour evolution and then introducing other relevant aspects.

    2. Title: the title refers to both complex plumage and island-dwelling, but the potential effects of complexity should apply regardless of being an island or mainland-dwelling species, am I right? Consider dropping the reference to islands in the title.

    3. The results encompass a large variety of statistical results some closely related to the main hypothesis (eg island/mainland differences) tested and others that seem more tangential (differences between body parts, sexes). Moreover, quite a few different approaches are used. I think that it would be good to be a bit more selective and concentrate the paper on the main hypotheses, in particular, because many results are not mentioned or discussed again outside the Results section.

    4. Related to the previous section, the variety of analytical approaches used is a bit bewildering and for the reader, it is unclear why different options were used in different sections. Again, streamlining would be highly desirable, and given the novel nature of the analytical approach (as far as I know, many analytical approaches are applied for the first time to study colour evolution) it would be good to properly explain them to the reader, highlighting their strengths and weaknesses.

    5. The Results section contains quite a bit of discussion (and methods) despite there being a separate Discussion section. I suggest either separating them better or joining them completely.

    6. The main analyses of colour evolutionary rates only include chromatic aspects of colour variation. Why was achromatic variation (i.e. light to dark variation) not included in the analyses? I think that such variation is an important part of the perceived colour (e.g. depending on their lightness the same spectral shape could be perceived as yellow or green, black or grey or white). I realize that this omission is not uncommon and I have done so myself in the past, but I think that in this case, it is highly relevant to include it in the analyses (also because previous work suggests that island birds are darker than their mainland counterparts). This should be possible, as achromatic variation may be estimated using double cone quantum catches (Siddiqi et al., 2004) and the appropriate noise-to-signal ratios (Olsson et al., 2018). Adding one extra dimension per plumage patch should not pose substantial computational difficulties, I think.

    7. The methods need to be much better explained. Currently, some methods are explained in the main text and some in the methods section. All methods should be explained in detail in the methods section and I suggest that it would be better to use a more traditional manuscript structure with Methods before Results (IMRaD), to avoid repetition (provided this is allowed by the journal). Whenever relevant the authors need to explain the choice of alternative approaches. Many functions used have different arguments that affect the outcome of the analyses, these need to be properly explained and justified. In general, most readers will not check the R script, and the methods should be understandable to readers that are not familiar with R. This is particularly important because I think that the methodological approach used will be one of the main attractions of the manuscript, and other researchers should be able to implement it on their own data with ease. Judging from the R script, there are quite a few analyses that were not reported in the manuscript (e.g. multivariate evolutionary rates being higher in forest species). This should be fixed/clarified.

  5. eLife

    Reviewer #2 (Public Review):

    In "Complex plumages spur rapid color diversification in island kingfishers (Aves: Alcedinidae)", Eliason et al. link intraspecific plumage complexity with interspecific rates of plumage evolution. They demonstrate a correlation here and link this with the distinction between island and mainland taxa to create a compelling manuscript of general interest on drivers of phenotypic divergence and convergence in different settings.

    This will be a fantastic contribution to the literature on the evolution of plumage color and pattern and to our understanding of phenotypic divergence between mainland and island taxa. A few key revisions can help it get there. This paper needs to get, fairly quickly, up to a point where the difference between plumage complexity and color divergence is defined carefully. That should include hammering home that one is an intraspecific measure, while one is an interspecific measure. It took me three reads of the paper to be able to say this with confidence. Leading with that point will greatly improve the paper if that point gets forgotten then the premise of the paper feels very circular.

    Also importantly, somewhere early on a hypothesized causal pathway by which insularity, plumage complexity, and color divergence interact needs to be laid out. The analyses that currently follow are good ones, and not wrong, but it's challenging to assess whether they are the right ones to run because I'm not following the authors' reasoning very well here. I think it's possible a more holistic analysis could be done here, but I'll refrain from any such suggestions until I better get what the authors are trying to link.

    We also need something near the top that tells us a bit more about the biogeography of kingfishers. Are kingfisher species always allopatric? I know the answer is no, but not all readers will. What I know less well though is whether your insular species are usually allopatric. I suspect the answer is yes, but I don't actually know.

    In short, how do the authors think allopatry/sympatry/opportunity for competition link to mainland vs. island link to plumage complexity? And rates of color evolution? Make this clear upfront.

  6. eLife

    Reviewer #3 (Public Review):

    In this article, the authors examined color evolution in the kingfishers, a group of birds that have achieved a spectacular diversity of colors and color patterns as they have diverged across the continents and island chains of the globe. Like many other avian taxa, kingfishers on islands often exhibit color patterns distinct from their close relatives. The authors focus here on putting this informally recognized pattern of evolutionary change to a formal test, asking if plumage color diversity and evolutionary rate are elevated on islands. They also explore whether a notable characteristic of some kingfishers - their simultaneous use of many of the coloration mechanisms available in birds - contributes to the evolutionary lability of their color patterns.

    The authors have previously explored how when color varies in birds it is not just in dimensions of color, but also in the distribution of those colors in patches on the body. Summarizing this variation is challenging, and there are statistical obstacles to comparing it in a holistic manner. In this study, the authors use an exceptional set of analyses to study color in total as a multivariate trait. These are the major strengths of the paper. The authors' efforts are somewhat less convincing when they pursue a univariate model fitting on a small number of principal components, but these analyses are not central to the study. And as with all studies using ancestral state reconstruction to test hypotheses, it's an important tool and one that contributes to this study's effectiveness, but we should acknowledge some level of uncertainty with its results.

    The authors report two important relationships in this study. They provide convincing evidence that rates of color evolution are elevated in island kingfishers, without convergence towards a particular island phenotype. They also describe a relationship between the complexity of plumage patterns and the rate at which they evolve, which has fundamental implications for our understanding of the tempo of trait evolution.

    Islands make up a tiny portion of the earth's surface but are home to a seemingly disproportionate amount of life's diversity. This paper makes an important contribution to our understanding of how this diversity is generated, by showing that the evolutionary rate is elevated on islands for traits relevant to mate choice and recognition. The authors find that "plumage complexity, rather than uniformity, provides more phenotypic traits for natural selection to act upon". Given the number of different coloration mechanisms they express, the kingfishers are a unique group in which to study this issue, so I look forward to reading and hearing more from the authors on this issue in the future.

  7. Version published to 10.1101/2022.09.26.509475v1 on bioRxiv