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Tempo and mode of morphological evolution are decoupled from latitude in birds

['Jonathan P. Drury', 'Department Of Biosciences', 'Durham University', 'Durham', 'United Kingdom', 'Julien Clavel', 'Natural History Museum', 'London', 'Univ. Lyon', 'Université Claude Bernard Lyon']

Date: 2021-09

The latitudinal diversity gradient is one of the most striking patterns in nature, yet its implications for morphological evolution are poorly understood. In particular, it has been proposed that an increased intensity of species interactions in tropical biota may either promote or constrain trait evolution, but which of these outcomes predominates remains uncertain. Here, we develop tools for fitting phylogenetic models of phenotypic evolution in which the impact of species interactions—namely, competition—can vary across lineages. Deploying these models on a global avian trait dataset to explore differences in trait divergence between tropical and temperate lineages, we find that the effect of latitude on the mode and tempo of morphological evolution is weak and clade- or trait dependent. Our results indicate that species interactions do not disproportionately impact morphological evolution in tropical bird families and question the validity of previously reported patterns of slower trait evolution in the tropics.

Here, we begin by expanding existing phylogenetic models of phenotypic evolution, including models that incorporate competition between species—namely, diversity-dependent (DD) models [ 19 , 20 ] and the matching competition (MC) model [ 22 , 43 ]—such that the impact of interactions between co-occurring lineages on trait evolution can be estimated separately in lineages belonging to different, predefined competitive regimes (e.g., tropical and temperate). We note that we use “competition” to encompass all processes (both direct and indirect), whereby trait evolution is impacted by co-occurring lineages. The models we develop are designed to account for known intraspecific variability and unknown, nuisance measurement error, both of which can strongly bias model support and parameter estimates [ 46 ]. In particular, it has been suggested that intraspecific variability is lower in the tropics [ 47 ], which could inflate estimates of evolutionary rates in the temperate biome. Next, we conduct a comprehensive test of the biotic interactions hypothesis using these new phylogenetic tools to model the effect of interspecific competition on the tempo and mode of morphological evolution based on 7 morphological characters describing variation in body size, bill size and shape, and locomotory strategies sampled from approximately 9,400 species representing more than 100 avian families worldwide. These morphological characters have been demonstrated to predict diet and foraging behavior in birds [ 48 ], indicating that they are well suited as proxies for analyzing the dynamics of ecological divergence.

Disentangling these opposing effects is challenging because previous macroecological studies have generally been restricted to either relatively few traits or limited samples of species. In addition, previous studies have been impeded by the lack of suitable methods for detecting the impact of species interactions on trait evolution [ 40 – 42 ], although recent progress has been made in developing such methods for use in standard comparative analyses [ 20 , 22 , 24 , 43 ]. By incorporating species interactions directly into phylogenetic models of trait evolution, these developments overcome some of the issues faced by phylogenetic and trait approaches for studying community assembly that rely on overly simplistic comparisons to randomly assembled communities [ 43 – 45 ]. However, these developments have not yet been deployed in the context of latitudinal sampling, and, thus, the key prediction of a latitudinal gradient in trait diversification has yet to be tested.

Whether competition predominantly drives or constrains divergence, the impacts on trait evolution should leave a detectable phylogenetic signature [ 22 – 25 ]. In addition, this signature should be most prevalent in the tropics, where each lineage interacts with far larger numbers of potential competitors. As such, the biotic interactions hypothesis predicts differences between tropical and temperate taxa in the pace of evolution (the “tempo,” in the parlance of comparative studies) and/or the processes that drive trait diversification (the “mode”). In comparison with the wealth of studies that have investigated latitudinal gradients in rates of species diversification [ 26 – 30 ], relatively few have tested for latitudinal gradients in the dynamics of phenotypic evolution and have mainly focused on tempo rather than mode. Their results so far suggest a potentially complex relationship between trait diversification and latitude. On the one hand, some studies have found greater divergence between sympatric sister taxa in body mass [ 31 ] and in plumage coloration [ 32 ] in the tropics, supporting the hypothesis that increased competition at lower latitudes drives character displacement [ 5 ]. On the other hand, some studies have found that species attain secondary sympatry after speciation more slowly in tropical regions [ 33 ] or that evolutionary rates are lower in the tropics for climatic niches [ 34 ], body size [ 34 , 35 ], or social signaling traits [ 34 , 36 – 39 ], implying that competition may limit ecological opportunity, and, therefore, constrain trait divergence in tropical regions.

In many groups of organisms, species richness increases toward lower latitudes—a pattern known as the latitudinal diversity gradient—inspiring generations of biologists to search for the causes and consequences of this gradient [ 1 ]. One hypothesis posits that species interactions are stronger in the tropics, and, therefore, play a more important role in many processes (e.g., diversification) in tropical lineages [ 2 – 6 ] (but see [ 7 ]). Previous tests of this “biotic interactions hypothesis” have generally focused on latitudinal gradients in the strength of ecological interactions between predator and prey, herbivore and plant, or pathogen and host [ 8 – 11 ]. Latitudinal gradients in the strength of competition between members of the same trophic level have been less explored, although they have been highlighted as one of the most important research directions for testing the biotic interaction hypothesis [ 5 ]. Competition among closely related species, such as those from the same taxonomic family, is often assumed to be strong since their ecological and phenotypic similarity increases the likelihood of competition for access to resources or space [ 12 – 16 ]. Such interactions can influence selection on traits that mediate access to resources, influencing trait evolution either by promoting divergence between lineages via character displacement [ 17 , 18 ] or, alternatively, by imposing constraints on geographical range overlap and ecological opportunity, reducing trait diversification as niches fill [ 19 – 21 ].

We found no evidence that territoriality or diet specialization are useful predictors of support for models that incorporate the impact of co-occurring species on phenotypic evolution ( S18 Table ). We did, however, find that the maximum proportion of species co-occurring on a continent (i.e., the maximum number of extant lineages on a single continent divided by the total clade size) had a pronounced impact on model selection—clades with a high proportion of lineages occurring on the same continent were more likely to be best fit by the MC model, whereas clades with a low proportion of co-occurring lineages were more likely to be best fit by the exponential DD model ( S13 and S14 Figs and S18 Table ). In addition, we found that the MC model was less likely to be favored in clades with many members living in single-strata habitats ( S18 Table ).

Phylogenetic models of competitively driven trait evolution rely on reconstructions of ancestral ranges to delimit the pool of potential species interaction at each point in the evolutionary history of a clade. Given the scale of our analyses and the computational limits of existing models of ancestral range estimation, we assumed that species occurring on the same continent were able to interact with one another. On average, species in our analyses are sympatric with 50% of clade members at the continental level, although there are differences across continents (mean range: 34% to 74%; S5 Fig and S9 and S10 Tables). Notably, we also found that temperate species are more likely to coexist in sympatry with family members than tropical species ( S11 Table ). To determine the impact of assuming continental scale sympatry, we investigated whether we would detect a latitudinal difference in the effect of competition on phenotypic evolution if it existed, even if competition occurs among only truly sympatric species rather than among all species occurring on the same continent. Simulations examining the impact of the continental scale sympatry assumption on the statistical power of 2-regime MC models demonstrate that, even for relatively small clades, large but biologically plausible latitudinal differences in the effect of competition should be detectable, even when sympatry is overestimated ( S8 Fig ). Nevertheless, there is evidence that this assumption can impact the power to detect subtle differences between regions and for smaller trees, the estimated direction of the difference ( S8 Fig ). However, restricting our empirical analyses to large clades (N ≧ 100), we still find no support for a consistently stronger impact of competition on phenotypic evolution in tropical lineages ( S8 Table ).

Estimates of slopes from (a) DD exp models and (b) DD lin models are not consistently different in tropical regions in any trait. (c) MC models estimated a decreased effect of competition in the tropics on bill pPC2. (d) Estimates of evolutionary rates from BM models show accelerated rates of locomotion pPC3, but not other functional traits, in temperate regions. Asterisks indicate statistical significance ( S7 and S14 Tables). For (a–c), each point represents the mean across clade-by-trait fits to stochastic maps of biogeography and of tropical/temperate membership (for all families with at least 50 species), and for (d), each point represents the mean across stochastic maps of tropical/temperate membership maximum (see S4 and S5 Datas). BM, Brownian motion; DD, diversity-dependent; DD exp , exponential diversity-dependent; DD lin , linear diversity-dependent; MC, matching competition; pPC, phylogenetic principal component.

There is no impact of latitude on the effect of competition on trait evolution as measured by the slope of (a) DD exp models or (b) DD lin models. (c) The effect of competition on trait evolution as measured by the repulsion parameter (“S”) from the MC models increases with the index of tropicality (the proportion of species in the clade with exclusively tropical breeding distributions) for locomotion pPC3 but not for other traits. (d) There is no relationship between the proportion of taxa in a clade that breed in the tropics and the estimated rate of trait evolution from BM models. Solid lines represent statistically significant relationships ( S6 and S13 Tables). For (a–c), each point represents the mean across clade-by-trait fits to stochastic maps of biogeography (for all families with at least 50 species), and for (d), each point represents the MLE for each clade-by-trait fit (see S2 and S3 Datas). BM, Brownian motion; DD, diversity-dependent; DD exp , exponential diversity-dependent; DD lin , linear diversity-dependent; MC, matching competition; MLE, maximum likelihood estimate; pPC, phylogenetic principal component.

We found no evidence for a latitudinal trend in the slope estimated from single-regime DD models ( Fig 2C and 2D and S6 Table ). However, the strength of repulsion estimated from single-regime MC models increased in more tropical families for locomotion pPC3 ( Fig 2B and S6 Table ). Parameter estimates from 2-regime models with competition (i.e., MC or DD models) do not support a stronger effect of biotic interactions on phenotypic evolution in the tropics ( Fig 3B–3D )—in most traits, there is no consistent difference between estimates of the impact of competition on tropical and temperate lineages, and in one case (bill pPC2), there is evidence that competition impacts temperate lineages to a larger degree than tropical lineages ( Fig 3B–3D and S7 Table ). In all cases, there was substantial variation in the fits, and the overall magnitude of differences between tropical and temperate regions was rather small ( Fig 3B–3D ).

There is no relationship between the proportion of taxa in a clade that breed in the tropics and statistical support (measured as the Akaike weight) for (a) BM, (b) OU, (c) EB models, (d) DD exp models, or (e) DD lin models. In MC models (f) , there is an increase in model support for locomotion pPC3 (solid line). The relative support for a model incorporating competition (i.e., MC or DD models) does not vary latitudinally for any trait ( S4 Table ). Each point represents the mean Akaike weight across clade-by-trait fits to stochastic maps of biogeography (i.e., each clade contributes a point for each of 7 traits; see S2 and S3 Datas). BM, Brownian motion; DD, diversity-dependent; DD exp , exponential diversity-dependent; DD lin , linear diversity-dependent; EB, early burst; MC, matching competition; OU, Ornstein–Uhlenbeck; pPC, phylogenetic principal component.

Across single-regime fits, we found no evidence for a latitudinal trend in the overall support for any model of phenotypic evolution ( Fig 1A–1F and S4 Table ), with one exception: There was an increase in model support for the MC model in tropical lineages for the locomotion phylogenetic principal component (pPC) 3 ( Fig 1F and S4 Table ). Similarly, there was no evidence that the overall support for models incorporating competition (i.e., MC or DD models) is higher in tropical clades ( Fig 1G and S4 Table ). Models with latitude (i.e., 2-regime models) were not consistently better supported than models without latitude, for any model or trait ( S5 Table ). Indeed, single-regime models were the best-fit models across 86% of individual clade-by-trait fits ( S7 Fig ).

We tested whether modes of phenotypic evolution varied with latitude using 2 types of models. First, we tested whether support for various “single-regime” models that estimate a single set of parameters on the entire avian phylogeny [ 26 ] varied according to a clade-level index of tropicality. Second, we developed and used “2-regime” models with distinct sets of parameters for tropical and temperate species and tested whether these latitudinal models were better supported than single-regime models.

Discussion

Contrary to what would be expected if the effect of competition on phenotypic evolution was stronger in the tropics, we did not find a consistent latitudinal gradient in the dynamics of phenotypic evolution across the entire avian radiation. Using novel methods for examining macroevolutionary signatures of the effect of competition on phenotypic evolution, we show that patterns of trait evolution across many clades are consistent with competition between clade members acting as an important driver of trait evolution. Nevertheless, we found no evidence that such competition has impacted the dynamics of trait diversification more in the tropics than in temperate regions. This lack of consistent latitudinal effect applied both to the support for specific models of phenotypic evolution and the parameters of these models. Our results contrast with several previous studies that have found a consistent signature of faster rates in the temperate biome [34,36–39,49].

The apparent absence of latitudinal patterns in support of phenotypic models with competition and estimates of competition strength did not arise from overall weak support for competition models, confirming previous findings that competition does leave a detectable signal in comparative, neontological datasets [22–25,50,51]. Indeed, models incorporating species interactions were the best-fit models in 25% of clade-by-trait combinations for single-regime fits. In sunbirds (Nectariniidae), for instance, the MC model was the best-fit model for body mass and 2 pPC axes describing variation in bill shape, suggesting that competition has driven trait divergence in this diverse clade. In owls (Strigidae), the exponential DD model was the best-fit model for body mass and several pPC axes describing bill shape and locomotory traits, suggesting that the rate of evolution in owls responds to changing ecological opportunity. The finding that interactions with co-occurring species commonly leave a signature on extant phenotypes in birds is echoed by a recent study showing that traits in a similar proportion of clades are best fit by competition models [50].

For both single-regime models and 2-regime models, we detected no systematic effect of latitude on the impact of competition on trait diversification. One possible explanation for this is that our approach was highly conservative since we assumed that species occurring on the same continent are likely to interact with one another, whereas they may be allopatric (with nonoverlapping geographical ranges) or exhibit low levels of syntopy within areas of sympatry [52]. However, previous work [23] and simulations exploring the impacts of assuming competition between potentially allopatric lineages suggest that the MC model is robust to some misspecification of geographic overlap (e.g., allopatric species scored as sympatric). This robustness is likely explained by both the imprint of competition on ancestral, coexisting lineages and a formulation of competition where divergence occurs respective to mean phenotypic values across interacting species (the mean across all species within each continent may be a relatively good proxy for the mean across sympatric species). Nevertheless, the possibility remains that, if differences between regions in the impact of competition are sufficiently small, the 2-regime models may not have detected them. In aggregate, however, our results consistently point to a conspicuous absence of a latitudinal gradient in the effect of competition on trait diversification.

One plausible explanation for discrepancies between our results and other studies that examine gradients in the tempo of morphological trait evolution is that our study accounted for observational error. Indeed, we found that overall observational error for body mass increased with latitude, and, when we intentionally ignored observational error, Brownian motion (BM) models were more likely to pick up faster rates of trait evolution at high latitudes. This result makes sense in the light of previously reported higher trait variance for temperate taxa [47] and a positive correlation between such variance and rate estimates [53]. Our analyses demonstrate that accounting for observational error when testing for latitudinal trends in evolutionary rates is crucial and also suggest that previous analyses overlooking error may have detected spurious latitudinal gradients in trait evolution.

Another potential explanation for the discrepancy between this and previous studies is that many previous studies examined gradients in rapidly evolving plumage and song traits, which may vary latitudinally if sexual or social selection is more pronounced in temperate regions [54]. In contrast, divergence in ecological traits is likely more constrained, as they tend to evolve relatively slowly [55,56].

A third explanation for the discrepancy is that many previous studies used sister taxa approaches to estimate gradients in trait evolution [34,36,37,49]. Yet, avian sister taxa are younger in temperate regions [33,49], and how these age differences influence rate estimates if trait evolution has proceeded in a non-Brownian fashion is not clear. Analyses on sister taxa of different ages can recover different rates even though these rates are not representative of any process unique to any particular region. For example, given that rates of trait evolution have accelerated toward the present [57], we may expect sister taxa to recover a signature of faster rates in temperate regions (where sister taxa are younger), even if there are no clade-wide latitudinal differences in the overall tempo and mode of evolution.

Within the competition models, the MC model was more likely to be chosen as the best-fit model than DD models, which is consistent with the notion that competition promotes divergence (e.g., via character displacement [17,18]) more often than it constrains divergence (e.g., via niche saturation [19]) at relatively shallow taxonomic scales [15,42,58]. Nevertheless, the possibility remains that other processes might generate patterns that are picked up by the MC and DD models. For instance, although the models we fit are designed to estimate the dynamics of trait evolution, competition can also generate patterns of divergence via its impacts on range dynamics (i.e., ecological sorting) when secondary sympatry is delayed by competitive interactions [21,59,60]. Therefore, although recent evidence suggests that the effects of competitive exclusion on community assembly is distinguishable from the action of character displacement in comparative datasets [25], the possibility remains that the MC model may detect a signal of ecological sorting of morphologically distinct lineages [21,61]—a process that is also fundamentally governed by competition—in addition to or instead of evolutionary divergence [25]. Further development of phylogenetic models that incorporate biotic interactions and simulation studies may help to clarify the processes that generate trait distributions which MC and DD models fit well.

In our analyses, we focused within clades, where we would expect competition to be strongest, owing to the phenotypic and ecological similarity of recently diverged taxa [16]. Nevertheless, in doing so, we excluded other competitors (e.g., nonfamily members with similar diets) that impose constraints on niche divergence. Such competitors have been shown to impact rates of trait evolution across clades of birds [53]. Future research could extend our approach by examining the impact of interactions between competitors from a wider diversity of clades.

We found evidence that support for the MC model was greater in clades with a higher proportion of lineages occurring on the same continent, suggesting that trait divergence may make coexistence possible [15,18]. The exponential DD model, on the other hand, was more likely to be the best-fit model in clades with relatively low levels of continental overlap, which may indicate that in these clades, niche saturation negatively impacts coexistence [62,63]. In addition, we found that model fits on clades with a high proportion of species living in single-strata habitats were less likely to favor the MC model, suggesting that opportunity for divergence may be limited in such habitats [64]. These relationships between ecological opportunity, trait evolution, and coexistence highlight the need for models that can jointly estimate the effects of diversification, range dynamics, and trait evolution [25,58]. Such models may identify an impact of competition on processes other than trait evolution, such as competitive exclusion, which may themselves vary latitudinally [21,33].

By including a suite of traits that capture functional variation in niches [48], we were able to identify patterns that would have been highly biased, or that we would have missed, by focusing on one specific trait, in particular body mass. Model support was distributed evenly across different traits, suggesting that the impact of competition varies both across clades and across different functionalities. For instance, while 31% (42/135) of clades exhibit some signature of competition acting on body size evolution in single-regime fits, 68% (92/135) of them exhibit some signature of competition acting on at least 1 of the 7 functional traits (body size, bill pPC axes, and locomotion pPC axes). These results further strengthen the notion that multiple trait axes are necessary to robustly test hypotheses about ecological variation [48,50,65].

We have extended various phylogenetic models of phenotypic evolution, including models with competition, to allow model parameters to vary across lineages (see also [51]) and to account for biogeography and sources of observational error. We then applied them to the case of latitudinal gradients, but they could be used to study other types of geographic (e.g., elevation), ecological (e.g., habitat and diet), behavioral (e.g., migratory strategy), or morphological (e.g., body size) gradients. Studies of gradients in evolutionary rates are often performed using sister taxa analyses, assuming BM or OU processes [66]. These analyses are useful because they enable quantitative estimates of the impact of continuous gradients on rate parameters. However, by limiting analyses to sister taxa datasets (and therefore ignoring interactions with other coexisting lineages), they are unable to reliably detect signatures of species interactions [67] and so cannot be used to study competition. In addition, these approaches are not well suited to differentiating between different evolutionary modes. Applying process-based models of phenotypic evolution that incorporate interspecific competition and biogeography allow for such tests of evolutionary hypotheses about the mode of trait evolution across entire clades.

Focusing on the effect of competition between closely related species on phenotypic evolution, we did not find support for the biotic interactions hypothesis. Biotic interactions are multifarious; individuals face selective pressures arising from competition, but also from other types of interactions such as predator–prey and host–parasite interactions. Perhaps as a result of this complexity, pinning down clear empirical relationships between latitude and biotic interactions has yielded a complex and often inconsistent set of results [7], with empirical evidence ranging from stronger interactions in the tropics [8,10] to stronger interactions in temperate regions [9]. A challenge for future research on the biotic interactions hypothesis is, therefore, to more precisely identify the mechanisms that lead to latitudinal gradients in interactions, and, consequently, better predict the kinds of interactions that may shape latitudinal gradients in diversification.

[END]

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