Bird clades with less complex appendicular skeletons tend to have higher species richness

Domain: earth_science
Published: 2023-09-19
Editorial outcome: minor_revision

Abstract
Species richness is strikingly uneven across taxonomic groups at all hierarchical levels, but the reasons for this heterogeneity are poorly understood. It is well established that morphological diversity (disparity) is decoupled from taxonomic diversity, both between clades and across geological time. Morphological complexity has been much less studied, but there is theory linking complexity with differential diversity across groups. Here we devise an index of complexity from the differentiation of the fore and hind limb pairs for a sample of 983 species of extant birds. We test the null hypothesis that this index of morphological complexity is uncorrelated with clade diversity, revealing a significant and negative correlation between the species richness of clades and the mean morphological complexity of those clades. Further, we find that more complex clades tend to occupy a smaller number of dietary and habitat niches, and that this proxy for greater ecological specialisation correlates with lower species richness. Greater morphological complexity in the appendicular skeleton therefore appears to hinder the generation and maintenance of species diversity. This may result from entrenchment into morphologies and ecologies that are less capable of yielding further diversity.

Introduction
There is a notoriously uneven distribution of species richness across the tree of life, with a disproportionately large number of species concentrated in a relatively small number of higher taxa. Indeed, the same marked asymmetry applies at all taxonomic levels, resulting in markedly imbalanced species distributions across sister groups1,2. The reasons for this asymmetry are poorly understood (but see refs. 3,4). Here, we explore the imbalance of species richness across extant bird groups, and test whether one aspect of their morphological complexity – the morphological differentiation of skeletal elements between fore and hind limbs – correlates with species richness across major avian clades. We follow McShea5–7 and McShea & Brandon8 in conceptualising biological complexity as a function of the number of elements comprising a structure, the grouping and organisation of those elements, and the relative differentiation between them. A system or structure comprising many parts that are greatly differentiated from one another is deemed more complex than a system or structure with fewer, homogeneous parts in a regular arrangement. While there is no universally agreed definition of complexity9–12, still less any single metric for its quantification13, systems with greater complexity typically also require more information to enable their description14, which our chosen conceptualisation of complexity satisfies. Complexity in this sense is solely a property of physical structure, and not of function. Form and function are inextricably linked, but complexity of form and complexity of function need not be5. Thus, we have no a priori expectation that any given ecology or life history should necessitate particular levels of morphological complexity.

The appendicular skeleton of birds is morphologically very diverse15–18. Birds also show a striking variation in species richness across clades of similar taxonomic rank or with the same most recent common ancestor19. For example, nearly 60% of living bird species are Passeriformes, whereas their sister clade – the Psittaciformes – encompass only 3.6% of extant avian diversity19–21 (Table 1). We note, therefore, that species richness is not necessarily expected to correlate with clade age22. The origin of birds from theropods, and the remarkable specializations in the appendicular skeleton that accompanied their subsequent radiation16,17,23, offer an excellent system for analysing the macroevolutionary relationships between diversity and complexity.

Morphological variety (disparity) is often a poor proxy for taxonomic diversity, and the decoupling of species richness (diversity) from the morphological disparity of species within clades or time bins is well established24. Most comparisons of diversity and disparity in macroevolutionary contexts have been implemented using palaeobiological data and feature extinct groups24–29, but there are also striking examples of decoupling in modern organisms. For example, extant afrotherian mammals have a modest diversity compared with many other mammalian clades, but also relatively high disparity: from elephants to elephant shrews, and from manatees to aardvarks. This disparity is reflected, for example, in terms of the wide variety of their vertebral formulae30. Clade disparity is therefore unlikely to offer much explanatory power for the heterogeneity of species numbers across clades, or vice versa.

Different modes of selection may have opposite effects upon species diversity within clades. Negative frequency-dependent selection31,32 tends to promote the evolution of greater diversity33, while stabilising selection tends to have a homogenising effect (e.g., ref. 34), thereby inhibiting diversification. Some theoretical models35,36 posit that more complex phenotypes have a greater probability of maintaining phenotypic diversity. Phenotypes with higher dimensionality (i.e., with more variable components) are considered to have greater complexity. If the interactions between those dimensions have an impact on fitness, the strength of negative frequency-dependent selection necessary to overcome stabilising selection is greatly reduced. This model has been extended to account for underlying ecological resource competition36, and supports the notion that adaptive diversification is more probable in complex phenotypes.

Theoretical work by Orr37 predicts that more complex organisms evolve and adapt more slowly than less complex organisms. However, whether this implies that groups of organisms with higher mean complexity diversify more slowly depends upon whether bursts of speciation and concurrent net diversification are adaptive or non-adaptive38. Whilst much diversification in birds is believed to be non-adaptive39, there are also some conspicuous adaptive radiations, including Darwin’s finches, Hawaiian honeycreepers40 and Madagascan vangas41. One possibility is that adaptive radiations occur more frequently in clades of lower complexity, owing to faster rates of adaptive evolution, and that these clades have greater species richness as a result. However, net diversification is as much a function of rates of extinction as of speciation. The link between Orr’s prediction and extinction rates could result from variable extinction risks, as more slowly adapting species are at greater risk in more rapidly changing environments42,43. Moreover, narrow habitat niches are associated with a greater extinction risk44, which is also consistent with specialists being at greater risk of diversity loss.

Differences in morphological complexity may, therefore, provide some explanation for uneven species richness, as greater complexity may promote more rapid diversification. Alternatively, greater morphological complexity may act as a hindrance to adaptive radiation and confer a greater risk of extinction, thereby acting as an inhibitor of rapid diversification. This leaves us with no clear consensus on what to expect from the empirical relationship between complexity and diversity. Here, we quantify an aspect of complexity in the avian appendicular skeleton, and address the null hypothesis that limb skeleton complexity is not correlated with the species richness of clades across living birds. Our investigation tests these hypotheses, utilizing the taxonomically, morphologically, and ecologically diverse radiation of these well-studied and iconic vertebrates.

In our model system, the fundamental axes of phenotypic variation are the lengths of the six major elements of the appendicular skeleton (excluding the phalanges): namely the femur, tibiotarsus, tarsometatarsus (hindlimb), humerus, ulna, and carpometacarpus (forelimb). Further axes of variation include the relative difference in length between limb pairs, and the relative proportions of equivalent elements (i.e., stylopod, zeugopod, and autopod) between limb pairs. Considered together, these variables allow us to index the “differentiation” component of morphological complexity (sensu refs. 5–8), with the number of constituent parts remaining constant. Whilst the number of elements is constant in our system, this need not always be the case. Different groups of arthropods, for example, can have highly divergent numbers of limb pairs. Differentiation here is analogous to the concept of morphological disparity. The key distinction is that in this case we refer to the morphological variation within a single individual, not across groups of species, as is the case with disparity.

A lack of complexity given our chosen definition is, therefore, exemplified by homogeneity. The lowest complexity scores (see Methods) will be achieved when both limb pairs are of the same length, with corresponding elements (stylopods, zeugopods, and autopods) between the two limbs being the same length. Importantly, this does not necessitate that elements within a limb are identical in length, merely that corresponding elements across the two limb pairs are identical. Hence, there are an unlimited number of ways of obtaining the minimum index of complexity, with stylopods, zeugopods and autopods of very different lengths and proportions, provided these are the same in both limb pairs.

The appendicular skeleton is an excellent study system for two reasons. Firstly, variability in limb skeleton morphology is broad and well documented15–17. Extant birds exhibit a wide range of proportional and size differences between limb pairs18, as do their extinct relatives45. Secondly, within- and between-limb differences in element proportions are frequently associated with ecological specialisation, and are underpinned by well understood development mechanisms46. One of the stipulations of some theoretical models35,36 is that axes of morphological variation must interact to influence the fitness of the whole organism in order to promote diversification. It is well established that limbs with different ecological or biomechanical functions often exhibit differences in the proportions of equivalent elements between limb pairs18,47,48, reflecting energetic trade-offs in development49. Further, functionally related elements of the avian limb skeleton show a signal of evolutionary integration50. This evolutionary, ecological, and ontogenetic intertwining of limb morphology is evidence that interactions between our axes of variation have an impact on fitness35,36, and that our metric of complexity, indexed as differentiation between the fore and hind limbs, has biological relevance.

Here, we show that the mean morphological complexity of the limb skeleton in bird clades correlates significantly and negatively with their species richness. Further, we find significant relationships between the foraging, trophic, and habitat niches occupied by species, and their complexity. Finally, we find that clades with greater mean complexity tend to occupy fewer ecological foraging niches, as well as being less species rich. These results suggest that greater morphological complexity acts as a hindrance to taxonomic diversification, potentially via greater ecological specialisation associated with those more complex phenotypes. Our results are also congruent with theoretical models suggesting that complexity will slow rates of adaptive evolution37, and are contrary to models suggesting complexity should enhance diversification35,36.

Results
Allometric variation can impact inferred complexity scores
Our index of complexity for a given species was derived as the Euclidean distance between fore and hind limbs in a three-dimensional morphospace, with one axis representing the lengths of each limb segment (stylopod, zeugopod, autopod), and each species therefore represented by two points (forelimb and hindlimb). Given the influence of body size upon many aspects of organismal biology, the removal of body-size related variation in bone lengths prior to further analysis was critical. We achieved this in two steps, one each to remove the effects of isometric and allometric variation. We first removed isometric size variation, that would otherwise inflate scores among larger-bodied species (see Methods; Supplementary Fig. 1), by expressing the length of each element as a proportion of the mean length for that species. We then applied a phylogenetic regression to these isometrically-transformed relative mean bone lengths, against body mass estimates for each species. From this we obtained phylogenetic residuals for each relative element length, independent of species body mass. This regression has the effect of removing allometric variation in relative bone lengths. Residual relative lengths of appendicular skeletal elements are highly variable across species, and between limb pairs (Fig. 1a–c). Data were compiled for a sample of 983 extant species (Supplementary Data 1).

Complexity scores derived in this way were found to exhibit no significant correlation with body mass in a phylogenetic generalised least-squares analysis (PGLS, p=0.3024, F=1.065 on 1 & 981 d.f., adjusted R2=6.588×10−5, N=983; Fig. 2a), confirming the successful removal of the influence of body size on inferred complexity scores.

Complexity scores derived directly from the isometrically-transformed values representing relative bone lengths, without the regression step to correct for allometry, were found to correlate

Methods

Peer review rounds
[{"round": 1, "reviewer_comments": {"reviewer_1": "In this paper the authors describe analyses of the link between morphological complexity and\ndiversity based on a substantial and broad sample across the extant avian tree of life. The results\nsuggest that there is a link between complexity and 1) the number of dietary and habitat niches\nand 2) species richness. In particular, species richness declines with increasing complexity.\nI enjoyed reading the manuscript and in particular the excellent scholarship around the core\nconcepts and predictions linking complexity to diversity. I have been introduced to an interesting\nrange of literature as a result. I found the premise of the paper fascinating and likely to be of\nbroad interest. However, I am not convinced that the data and metric used as a proxy for\ncomplexity are adequate. Broadly, complexity describes the number of parts and differentiation of\nthose parts. The metric here (in simple terms) describes relative proportions and differences\namong limb length pairs. The lowest complexity score arises when all of the six measured bones\nare the same length. But, biologically, it is not at all clear that this is relevant. From a\ndevelopmental or genetic perspective it is difficult to understand why equal bone lengths represent\nmore complex processes than bones of unequal length. Similarly, there is no reason to assume\nfrom an ecological perspective that equal bone lengths are more complex than unequal lengths.\nThe limb length proportion metric may well capture something interesting biologically - indeed the\nphylogenetic distribution of the complexity score suggests that there may be some ecological\nrelevance. The problem is that there is a lack of justification for referring to this as complexity. A\ncase could be made that complexity is partially related to dispersal. The most complex taxa seem\nto be large, long legged groups that may be poor dispersers or longer winged species that are\nwide dispersers. In this sense complexity may reflect extremes of dispersal ability with low\ncomplexity associated with intermediate dispersal. It may then be that the illustrated link between\nthe metric of complexity and species richness is revealing something about correlation between\nintermediate dispersal ability and speciation.\nMeasuring complexity is clearly challenging and directly addressing whether a given metric\nis a good proxy for complexity may not be possible. However, I do think it is important to 1)\nmore strongly justify why this is a relevant metric to use for measuring complexity and 2)\nexamine\nwhether the metric is associated with other traits in more depth. As highlighted above, one such\ntrait is dispersal but it would also be helpful to understand broader links to ecology and life history.\nWithout this deeper understanding of what the complexity score measures, it is not possible to\nadequately interpret what is potentially a very interesting relationship.\nMinor comments\nLine 421: phylogenetic signal was estimated with K. I assume that this is Blomberg’s K, if so the\npaper should be cited (https://onlinelibrary.wiley.com/doi/10.1111/j.0014-3820.2003.tb00285.x).\nA picky point, K is a statistic rather than a parameter.", "reviewer_2": "Paper Review Nature Comms 391737\nThis paper quantifies the relationship between complexity and diversity across extant bird clades\nwith an impressive dataset of nearly 1000 species, demonstrating a negative correlation between\nmorphological complexity and taxonomic diversity. This is an interesting finding and grows our\nunderstanding of the factors that influence differential diversity across the tree of life. With only\nminor revisions this will be an excellent contribution to Nature Communications.\nThe authors claim to test two alternative hypotheses, first that complexity is positively correlated\nwith richness because it promotes more rapid diversification and second that complexity is\nnegatively correlated with diversity because it confers greater risk of extinction. Because they are\ntesting the correlation between complexity and richness and not complexity~speciation rate nor\ncomplexity~extinction risk, I think it would be better to reduce the text hypothesizing mechanisms\ndriving either pattern until the discussion section. Indeed, in the discussion you hypothesize that\nthe negative complextity/richness pattern is explained by “complex species should be slower to\nevolve and adapt” rather than extinction risk\nIt is clear from Figure 4 that Passeriformes is a major outlier for log(species richness). I used\nthe supplemental code to re-run the analyses with this clade removed and I was happy to see that the\noverall relationship between diversity and complexity was unchanged. I think it would be good to\nacknowledge this outlier and that it is not strongly biasing the results in the main manuscript text.\nOn line 89 you say: “Considered together, these variables allow us to index both the\n“differentiation” and “arrangement” components of morphological complexity (sensu [5-8]), with\nthe number of constituent parts remaining constant. “ After this part of the manuscript you never\nagain return to arrangement component, instead focusing only on arrangement. I think it would be\nbest to focus only on differtaition in the introduction.\nLine 66-67: “including Darwin’s finches and Hawaiian honeycreepers, and Madagascan vangas”\nshould be “including Darwin’s finches, Hawaiian honeycreepers, and Madagascan vangas [40,41].”.\nthe comma is necessary as the finches are Darwin's but the honeycreepers are not.\nLine 89: I think it would be helpful to define “differentiation” and “arrangement” in the present\npaper\nThere seems to be a small problem with the supplemental R code file. On lines 119 and 120 I get\nthe following error message:\nError in which(rownames(logged_lengths_phylmod$resid) == names(logged_comp_scores)[i]) :\nobject 'logged_comp_scores' not found\nIt looks like you are calling an object named “logged_comp_scores” that was never defined.\nDouble check before submitting."}, "author_response": "Response to Reviewers’ Comments\nReviewer 1\n• “In this paper the authors describe analyses of the link between morphological complexity\nand diversity based on a substantial and broad sample across the extant avian tree of life.\nThe results suggest that there is a link between complexity and 1) the number of dietary and\nhabitat niches and 2) species richness. In particular, species richness declines with increasing\ncomplexity.”\nYes, this is a fair and accurate statement of the scope of our study, and of our key findings.\n• “I enjoyed reading the manuscript and in particular the excellent scholarship around the core\nconcepts and predictions linking complexity to diversity. I have been introduced to an\ninteresting range of literature as a result. I found the premise of the paper fascinating and\nlikely to be of broad interest.”\nWe sincerely thank the referee for their kind words.\n• “However, I am not convinced that the data and metric used as a proxy for complexity are\nadequate. Broadly, complexity describes the number of parts and differentiation of those\nparts.The metric here (in simple terms) describes relative proportions and differences among\nlimb pairs. The lowest complexity score arises when all of the six measured bones are the\nsame length. But, biologically, it is not at all clear that this is relevant.”\nThe referee highlights some ambiguity in our writing – we have recast this for much greater clarity.\nThe referee is also correct, that the score is at a minimum if “all of the six measured bones are the\nsame length”. However, the identity of all six bones is not what is being measured here, but rather\nthe difference between fore and hindlimbs (which will be zero if all bones are identical). Importantly,\nthe minimum score can also be achieved when there is heterogeneity within limbs, but both limb\npairs are of exactly equal length and proportions. We therefore treat fore- and hindlimbs as serial\nhomologues, and are interested in the extent to which they are differentiated. Differences between\nthe lengths of bones within a limb do not contribute directly to the indices, other than to the extent\nthat these contrast with the lengths of the elements in the other limb pair. Differentiation between\nlimb pairs has well established biological implications (we detail this in the manuscript, with\nreferences cited).\n• “From a developmental or genetic perspective it is difficult to understand why equal bone\nlengths represent more complex processes than bones of unequal length.”\nAs above, our original explanation was not clear enough, and we have rewritten the relevant\nsections. Our null assumption is for homogeneity wherever elements (limb pairs, bones, genes, etc)\narise by duplication or are otherwise homologous. Our serial homologues are the limbs, not the\nbones within a limb. Such homogeneity characterises low (rather than high) complexity. The zero-\nforce evolutionary law (McShea & Brandon, 2010) conceptualises complexity in this way.\nDevelopmental differences underpin the differentiation that leads to greater complexity, and these\ndifferences are known and understood in birds. We have expanded the text, and cited a recent\nreview of limb development which includes avian case studies (line 114).\n• “Similarly, there is no reason to assume from an ecological perspective that equal bone\nlengths are more complex than unequal length. The limb length proportion metric may well\ncapture something interesting biologically - indeed the phylogenetic distribution of the\ncomplexity score suggests that there may be some ecological relevance. The problem is that\nthere is a lack of justification for referring to this as complexity.”\nWe should have discussed possible relationships between morphological complexity (which all our\nindices seek to capture) and functional complexity in our manuscript. There is no expectation that\nmorphological and functional complexity should be correlated. We have added a section justifying\nour distinction between morphological complexity and functional complexity at lines 34-39. Despite\nthis theoretical separation, we do recover a significant relationship between complexity and various\nproxies for ecology, implying that our metric does capture morphological variation in an ecologically\nrelevant manner. We cite several references in the manuscript which show evidence of the impact of\nlimb lengths and proportions on various aspects of ecology and life history.\n• “A case could be made that complexity is partially related to dispersal. The most complex\ntaxa seem to be large, long legged groups that may be poor dispersers or longer winged\nspecies that are wide dispersers. In this sense complexity may reflect extremes of dispersal\nability with low complexity associated with intermediate dispersal. It may then be that the\nillustrated link between the metric of complexity and species richness is revealing something\nabout correlation between intermediate dispersal ability and speciation.”\nThis is entirely possible, although not something we set out to address in our original manuscript.\nWhile we do not have data on dispersal ability per se, we were able to collect data on Kipp’s distance\n(the distance between the tip of the first secondary flight feather and the tip of the longest primary\nflight feather) as a first approximation. This has been used in models elsewhere, in conjunction with\nother variables, as a proxy for dispersal ability (Dawideit et al., 2009). We have added an additional\nPGLS analysis in the Results (lines 192-199) and Materials & Methods (lines 482-487) sections\n(including a new Supplementary Figure), and a more explicit examination of this possibility in the\nDiscussion section at lines 309-317. This expands on the original text. We stress that model fit is very\npoor, likely reflecting the complexity of the relationship and the influence of many other variables\nfor which we do not have data. A great deal of further work, well beyond the scope of this study,\nwould be needed to unpack it.\n• “Measuring complexity is clearly challenging and directly addressing whether a given metric\nis a good proxy for complexity may not be possible. However, I do think it is important to 1)\nmore strongly justify why this is a relevant metric to use for measuring complexity…”\nSee above points, and additions/alterations to the manuscript at lines 34-39 and 114.\n• “… and 2) examine whether the metric is associated with other traits in more depth. As\nhighlighted above, one such trait is dispersal but it would also be helpful to understand\nbroader links to ecology and life history. Without this deeper understanding of what the\ncomplexity score measures, it is not possible to adequately interpret what is potentially a\nvery interesting relationship.”\nThis would entail an enormous amount of additional data collection and modelling, as few such\ntraits are consistently quantified at this level of sampling. This would effectively entail writing an\nentirely new paper. As detailed above, we have added an additional analysis and Supplementary\nFigure measuring the correlation between complexity and Kipp’s distance (a weak proxy for dispersal\nability). What the reviewer suggests is certainly a good prospect for future investigations.\n• “Line 421: phylogenetic signal was estimated with K. I assume that this is Blomberg’s K, if so\nthe paper should be cited (https://onlinelibrary.wiley.com/doi/10.1111/j.0014-\n3820.2003.tb00285.x). A picky point, K is a statistic rather than a parameter.”\nA citation of Blomberg et al.’s paper has been added where a K statistic is first reported on lines 161-\n162. References to K as a parameter have been altered to refer to it as a statistic (these on lines 468\nand 475).\nReviewer 2\n• “This paper quantifies the relationship between complexity and diversity across extant bird\nclades with an impressive dataset of nearly 1000 species, demonstrating a negative\ncorrelation between morphological complexity and taxonomic diversity. This is an interesting\nfinding and grows our understanding of the factors that influence differential diversity across\nthe tree of life. With only minor revisions this will be an excellent contribution to Nature\nCommunications.”\nThis is an accurate statement of our central goal and finding, and we thank the reviewer for their\nkind words.\n• “The authors claim to test two alternative hypotheses, first that complexity is positively\ncorrelated with richness because it promotes more rapid diversification and second that\ncomplexity is negatively correlated with diversity because it confers greater risk of extinction.\nThe second alternative is related to a theoretical work by Orr (2000). That work pertains only to the\nrate of adaptive evolution, and as such could relate to either speciation or extinction rates. We state\nthat this could impact diversity in more complex clades by either slowing the rate of diversification,\nor increasing the risk of extinction, or both. Whether one of these mechanisms is prevalent over the\nother in this sample is not currently clear, and so in the Discussion we do not attempt to make direct\nlinks to either process (see next comment). We instead explain our findings in the context of their\ncongruence to Orr’s original models, which assess only rates of adaptive evolution.\n• Because they are testing the correlation between complexity and richness and not\ncomplexity~speciation rate nor complexity~extinction risk, I think it would be better to reduce\nthe text hypothesizing mechanisms driving either pattern until the discussion section. Indeed,\nin the discussion you hypothesize that the negative complextity/richness pattern is explained\nby “complex species should be slower to evolve and adapt” rather than extinction risk”\nThis is a fair point, but we hesitate to remove it from the Introduction, as we consider it to be key in\nformulating and justifying the alternative hypotheses we propose. The reviewer is correct in stating\nthat we do not directly assess the relationship between either speciation or extinction rates, which\nwe acknowledge in the Discussion as a major opportunity for future work.\n• “It is clear from Figure 4 that Passeriformes is a major outlier for log(species richness). I used\nthe supplemental code to re-run the analyses with this clade removed and I was happy to see\nthat the overall relationship between diversity and complexity was unchanged. I think it\nwould be good to acknowledge this outlier and that it is not strongly biasing the results in the\nmain manuscript text.”\nThis is an excellent point. We have changed the Results section at lines 165-169 to acknowledge\nPasseriformes as an outlier, and provide summary statistics obtained from repetition of model-\nfitting with passerines excluded. Further summary statistics and parameters from this refitted model\nhave been appended to SI Table 4 in the Supplementary Information document.\n• “On line 89 you say: ‘Considered together, these variables allow us to index both the\n‘differentiation’ and ‘arrangement’ components of morphological complexity (sensu [5-8]),\nwith the number of constituent parts remaining constant.’ After this part of the manuscript\nyou never again return to arrangement component. I think it would be best to focus only on\ndifferentiation in the introduction.”\nWe have removed sections of the text referring exclusively to “arrangement” from the Introduction.\nWe concur that this makes for a clearer and more streamlined paper.\n• “Line 66-67: “including Darwin’s finches and Hawaiian honeycreepers, and Madagascan\nvangas” should be “including Darwin’s finches, Hawaiian honeycreepers, and Madagascan\nvangas.”\nAgreed. This alteration has been made at line 72.\n• “Line 89: I think it would be helpful to define “differentiation” and “arrangement” in the\npresent paper.”\nAn excellent point. We have added text at lines 99-101. “Differentiation” as applied to serially\nhomologous structures within an individual organism is analogous to the disparity of species within a\nclade, and could be quantified using the same indices as deployed for the latter purpose. As\n“arrangement” is no longer discussed we do not provide a working definition for it.\n• “There seems to be a small problem with the supplemental R code file. On lines 119 and 120 I\nget the following error message:\nError in which(rownames(logged_lengths_phylmod$resid) ==\nnames(logged_comp_scores)[i]) : object 'logged_comp_scores' not found\nIt looks like you are calling an object named “logged_comp_scores” that was never defined.\nDouble check before submitting.”\nThis reported bug has been checked and fixed. The object was defined as “logged_scores”, then\ncalled as “logged_comp_scores”. It is now consistently referred to as “logged_comp_scores”."}, {"round": 2, "reviewer_comments": {"reviewer_1": "In the revised manuscript and response letter the authors have clarified a number of points around\nthe complexity measure and its meaning, correcting misunderstandings on my part. I am now far\nmore convinced by their choice of metrics. Given this greater clarity, my other suggestion around\nthe association of the complexity with other metrics is much less important and I agree with the\nauthors that it is not necessary for this manuscript. I have a small number of minor suggestions,\nincluding one additional (but straightforward) analysis but otherwise .\n1. Lines 49-50: the authors suggest that most comparisons of diversity and disparity have been\nimplemented in a palaeo context. I agree that this is largely true in a macroevolutionary context\nbut in ecology there are many studies in a spatial context of functional diversity and species\nrichness. Functional diversity and disparity are the same metric (or toolbox of metrics) but given\ndifferent names in different disciplines. This is a longwinded way of suggesting being explicit about\nthe macroevolutionary context in this sentence.\n2. Line74-75: The authors suggest that Orr’s prediction is more intuitively linked to extinction than\nspeciation. This is subjective and it could be argued that the link to speciation is intuitive in the\ncontext of Schluter’s idea of evolution along line of least resistance.\n3. Line 94: extra word - remove “but”\n4. Section beginning line 215: there are strong positive correlations between measures of habitat\nor niche diversity and species richness. This seems inevitable by chance alone (small clades cannot\nattain the highest levels of niche diversity). The null expectation is not of no relationship. A rough\nnull expectation could be derived by random shuffling of niche and habitat among tips (species)\nand then recalculating clade niche and habitat diversity. This randomisation can be repeated and\nused to establish a null expectation for relationship between niche number and species richness.\nThis would give context to the observed results.", "reviewer_2": "The authors have adequately addressed the concerns raised by the reviewers in the previous\nround of reviews. I will be happy to see this accepted and published."}, "author_response": "Response to Reviewers’ Comments\nReviewer 1\n“In the revised manuscript and response letter the authors have clarified a number of points around\nthe complexity measure and its meaning, correcting misunderstandings on my part. I am now far\nmore convinced by their choice of metrics. Given this greater clarity, my other suggestion around the\nassociation of the complexity with other metrics is much less important and I agree with the authors\nthat it is not necessary for this manuscript. I have a small number of minor suggestions, including one\nadditional (but straightforward) analysis but otherwise .”\n• We are glad that we were able to improve the clarity of the manuscript, and thank the\nreviewer for bringing these points to our attention. This has undoubtedly improved the\nquality of the work greatly.\n“1. Lines 49-50: the authors suggest that most comparisons of diversity and disparity have been\nimplemented in a palaeo context. I agree that this is largely true in a macroevolutionary context but\nin ecology there are many studies in a spatial context of functional diversity and species richness.\nFunctional diversity and disparity are the same metric (or toolbox of metrics) but given different\nnames in different disciplines. This is a longwinded way of suggesting being explicit about the\nmacroevolutionary context in this sentence.”\n• We have added to the relevant text (lines 49-50) to make clear that we are referring solely\nto studies in a macroevolutionary context.\n“2. Line74-75: The authors suggest that Orr’s prediction is more intuitively linked to extinction than\nspeciation. This is subjective and it could be argued that the link to speciation is intuitive in the\ncontext of Schluter’s idea of evolution along line of least resistance.”\n• This point is fairly made, and we have removed the subjective language. This has been\nreplaced by a more direct statement, avoiding any notion of intuition (line 76).\n“3. Line 94: extra word - remove “but””\n• The extra word has been removed.\n“4. Section beginning line 215: there are strong positive correlations between measures of habitat or\nniche diversity and species richness. This seems inevitable by chance alone (small clades cannot\nattain the highest levels of niche diversity). The null expectation is not of no relationship. A rough null\nexpectation could be derived by random shuffling of niche and habitat among tips (species) and then\nrecalculating clade niche and habitat diversity. This randomisation can be repeated and used to\nestablish a null expectation for relationship between niche number and species richness. This would\ngive context to the observed results.”\n• We have done as the reviewer suggested, and implemented a randomisation-like approach,\nwhereby tip values for each of the three categorical variables are randomly reassigned into\ngroups of the same number and sizes as the empirical observations. Refitting of the PGLS\nmodels across 1,000 permutations of each variable revealed that significant positive\ncorrelations are indeed the null expectation, as the reviewer suspected. We agree that this\ndoes provide useful context for this section of the Results. Additional text has been added in\nthe Results (lines 226-264), Discussion (lines 321-322), and Materials & Methods (lines 521-\n538) sections, as well as three new supplementary figures (SI Figs. 5-7).\nReviewer 2\n“The authors have adequately addressed the concerns raised by the reviewers in the previous round\nof reviews. I will be happy to see this accepted and published.”\n• No new points need addressing from this reviewer’s response. We are glad that we were\nable to adequately respond to and solve their previous concerns, and thank them for the\nimprovements to this work which their comments elicited."}]

Decision letter