Phylogenetic scale in ecology and evolution

Department of Ecology and Evolution, Stony Brook University, Stony Brook, New York Biodiversity and Conservation Biology Unit, Swiss Federal Research Center (WSL), Birmensdorf, Switzerland Department of Ecology, Faculty of Science, Charles University, Prague 2, Czech Republic Center for Theoretical Study, Charles University, Prague 1, Czech Republic Center for Macroecology, Evolution and Climate, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark

SUMMARY It has been widely acknowledged that many phenomena in ecology and evolution 23 depend on spatial and temporal scale. However, important patterns and processes may vary also 24 across the phylogeny and depend on phylogenetic scale. Though phylogenetic scale has been 25 implicitly considered in some previous studies, it has never been formally conceptualized and its 26 potential remains unexplored. Here, we develop the concept of phylogenetic scale and, building 27 on previous work in the field, we introduce phylogenetic grain and extent, phylogenetic scaling 28 and the domains of phylogenetic scale. We use examples from published research to demonstrate 29 how phylogenetic scale has been considered so far and illustrate how it can inform, and possibly 30 resolve, some of the longstanding controversies in evolutionary biology, community ecology, 31 biogeography and macroecology. To promote the concept of phylogenetic scale empirically, we 32 propose methodological guidelines for its treatment. The concept of phylogenetic scale seems particularly pertinent, given the growing body 80 of research and statistical methods to explore the increasingly accurate and ever more complete 81 phylogenetic data (e.g. phylogenetic comparative methods, community phylogenetics, 82 . CC-BY-NC-ND 4.0 International license a certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under The copyright holder for this preprint (which was not this version posted July 27, 2016. ; https://doi.org/10.1101/063560 doi: bioRxiv preprint diversification analysis). Yet, few studies have extended the explorative strategies to 83 systematically investigate phylogenetic scale-dependence (e.g. upscaling, downscaling), delimit 84 phylogenetic domains of ecological theories (e.g. niche conservatism, competition and filtering, 85 equilibrial diversification), or evaluate the universal laws of ecology (e.g. species-abundance 86 distributions, latitudinal gradients). We therefore contend that the full potential of the 87 phylogenetic data and the methods at hand has not yet been realized, and further progress might 88 be precipitated by a more focused and formalized treatment of phylogenetic scale, akin to the one 89 commonly applied across temporal and spatial scales (e.g. Wiens 1989; Levin 1992; Schneider 90

2001). 91
Here, we summarize the variety of ways in which different disciplines have considered 92 phylogenetic scale, highlighting their respective benefits and pitfalls. We further propose how 93 these efforts might be consolidated under one conceptual and empirical framework that would 94 provide the common ground for cross-disciplinary discussion. In particular, we define the 95 concept of phylogenetic scale, distinguish between phylogenetic grain and extent, scale-96 dependence, phylogenetic scaling and the domains of scale. We also provide practical guidelines 97 for the treatment of phylogenetic scale across empirical studies, using the data and statistical 98 methods currently available. We hope this will inspire further discussion, draw more focused 99 attention to the subject, and advance the notion of phylogenetic scale in ecology and evolution. 100

PHYLOGENETIC SCALE IN ECOLOGY AND EVOLUTION 102
Phylogenetic scale has been considered to varying degrees in ecology and evolution, from being 103 largely neglected to being relatively well-developed. In this section, we describe previous 104 research that has implicitly or explicitly considered phylogenetic scale but also how the core 105 disciplines in the field might further benefit from this concept (e.g. macroevolution, community 106 ecology, biogeography, macroecology). 107 108 109 110 111 . CC-BY-NC-ND 4.0 International license a certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under The copyright holder for this preprint (which was not this version posted July 27, 2016. ; https://doi.org/10.1101/063560 doi: bioRxiv preprint  . CC-BY-NC-ND 4.0 International license a certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under The copyright holder for this preprint (which was not this version posted July 27, 2016. ; https://doi.org/10.1101/063560 doi: bioRxiv preprint 6 BOX 1: The concept of phylogenetic scale 122 The concept of scale is based on the fact that some entities can be ordered, or placed on a scale 123 (scala means ladder in Latin). For example, continents contain biomes, ecoregions, and localities, 124 giving rise to spatial hierarchy. Similarly, large clades contain small clades, creating phylogenetic 125 hierarchy which defines phylogenetic scale. However, clades are not always nested, in which case 126 standard measures might be needed to order the clades along the scale continuum. These 127 measures might include time (clade age) but also clade size (number of species within a clade) or 128 the degree of molecular, phenotypic, or ecological divergence within a clade. These measures will 129 be inherently correlated across mutually nested clades but might become decoupled across non-130 nested clades (e.g. old clades will not necessarily be most diverse) (Box 2). 131 In the concept of spatial scale, grain and extent are usually distinguished. Grain refers to the area 132 of the basic unit analyzed (e.g. ecoregion) while extent refers to the total area analyzed (e.g. 133 continent). Phylogenetic scale can be defined analogically, such that phylogenetic grain refers to 134 the basic unit of analysis (e.g. species, genera, families) and phylogenetic extent to the total 135 phylogeny that would encompass all the units analyzed (e.g. class, phylum). CC-BY-NC-ND 4.0 International license a certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under The copyright holder for this preprint (which was not this version posted July 27, 2016. ; https://doi.org/10.1101/063560 doi: bioRxiv preprint Even though taxonomic ranks are commonly used to define phylogenetic scale, they are not 151 always comparable (e.g. genera in mammals are not comparable to genera in insects), and 152 standard measures might be better suited to define phylogenetic scales across distant taxa (e.g. 153 taxon age, taxon size), but even these measures might not ensure entirely that the analyzed taxa 154 are fully comparable. For example, clade age might reflect the degree of phenotypic divergence 155 across clades, but some clades might be more diverged than others despite being of similar age. 156 The same limitations apply to the measures of spatial scale because spatial grains of standardized 157 sizes might not ensure comparability across species of dramatically different geographic and 158 home range sizes (Wiens 1989). Therefore, the most suitable measure and definition of the 159 phylogenetic scale should be dictated by the biological properties of the organismal system (e.g. 160 body size, generation time, rates of phenotypic evolution) and the question under study (e.g. 161 phenotypic divergence, diversification dynamics, diversity patterns). 162 In some cases, it may be useful to work with non-standardized grains which represent more 163 natural units of analysis (e.g. islands in spatial scaling or island faunas in phylogenetic scaling). 164 The extents will then be defined correspondingly, so as to cover all of the units analyzed (e.g. all 165 islands or the entire biotas across islands). Finally, grain and extent are defined only in relation 166 to each other. The grain from one study can therefore act as an extent in another study, or vice  Table 1), most studies report the recovered patterns without a focused examination 175 of their scale-dependence. Focused examination of patterns across scales may precipitate the 176 resolution of several outstanding controversies in the field. 177 One such controversy revolves around the dynamics of diversity and diversification. It 178 has been debated whether the dynamics are expansionary, such that regional and clade diversity 179 These mixed results suggest that temporal scale may be insufficient to fully capture the 209 variance in niche conservatism. Phylogenetic scale, in contrast, captures the fact niches and traits 210 . CC-BY-NC-ND 4.0 International license a certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under The copyright holder for this preprint (which was not this version posted July 27, 2016. ; https://doi.org/10.1101/063560 doi: bioRxiv preprint may evolve at different rates even across closely related clades (e.g. due to clade-specific selection 211 regimes, genetic architecture, pleiotropy) that span similar temporal scales but different 212 phylogenetic scales (e.g. one clade has undergone an explosive radiation on an island while the 213 other has accumulated only limited morphological, ecological, and species diversity on the 214 mainland). In these cases, time will not capture the phylogenetic hierarchy as well as phylogenetic 215 scale would (e.g. phylogenetic domains defined to reflect clade size, phenotypic and ecological 216 divergence) (see below). The concept of phylogenetic scale may therefore encourage a more 217 realistic and potentially more accurate way of thinking about trait evolution and niche 218 conservatism. 219 220

Community ecology 221
Patterns of community phylogenetic structure, and hence the inferred processes that shape To study the phylogenetic structure of a community, researchers calculate standardized 227 community metrics (e.g. the net relatedness index, NRI) based on null models which assemble 228 random communities from the regional pool of species. Phylogenetic delimitation of the species 229 pool can influence these metrics profoundly and inform us about the mechanisms that mediate sufficiently to identify the processes that produced the community (Gerhold et al. 2015). We argue 240 . CC-BY-NC-ND 4.0 International license a certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under The copyright holder for this preprint (which was not this version posted July 27, 2016. ; https://doi.org/10.1101/063560 doi: bioRxiv preprint that using multiple metrics across phylogenetic scales, as illustrated by some recently developed 241 and about the mechanisms (e.g. mathematical, geometric, random sampling, or biological) that 296 likely produced them (Marquet et al. 2004;McGill 2008). 297 Some of the patterns originally considered to be universal have later been reported to 298 disintegrate across phylogenetic scales. The latitudinal diversity gradient provides a very 299 intuitive example, where the pattern holds across most higher taxa (e.g. mammals, birds, 300 . CC-BY-NC-ND 4.0 International license a certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under  (Fig. 1a). Likewise, species 304 abundance and body mass are negatively correlated across birds and mammals (Damuth 1981), 305 but the correlation disappears across narrowly defined taxa (Isaac et al. 2011) and becomes even 306 positive in some tribes of birds (Cotgreave 1994) (Fig. 1b). These changes in correlation 307 coefficients across phylogenetic scales implicate the mechanisms behind the correlation. Within 308 large phylogenetic extents, small-bodied species are locally abundant because their low metabolic 309 requirements raise the carrying capacities of their populations (Gaston and Blackburn 1997). 310 However, within restricted extents, local abundance becomes constrained by competition 311 between closely related species, and large-bodied species become locally abundant because of 312 their competitive superiority, thus reversing the directionality of the correlation between body 313 size and population abundance across phylogenetic scales (Cotgreave 1994) (Fig. 1b). 314

Moreover, the species-area relationship (SAR) and species-abundance distribution (SAD) 315
were traditionally believed to universally conform to certain mathematical forms (the power-law 316 function and the lognormal distribution, respectively) (Preston 1948;Rosenzweig 1995). The fact that some statistical patterns disintegrate across phylogenetic scales implies that 324 the theories to explain these patterns, based on the universal principles of geometry and 325 mathematics, might be fundamentally ill-founded (Storch & Šizling 2008). It is also possible that 326 the theories pertain to certain phylogenetic scales only. This would suggest that phylogenetic 327 scales form phylogenetic domains (Box 2) within which the processes hypothesized by our 328 theories operate. However, the boundaries of these phylogenetic domains remain largely 329 unexplored, and their empirical delimitation might further inform the theory (see Box 2). 330 . CC-BY-NC-ND 4.0 International license a certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under The copyright holder for this preprint (which was not this version posted July 27, 2016. ; https://doi.org/10.1101/063560 doi: bioRxiv preprint 13 BOX 2: Research across phylogenetic scales 331 Many attributes, such as diversification rate, niche conservatism, or community structure, vary 332 across phylogenetic scales (Table 1). They may vary in three different ways: 333 (a) Scale dependence refers to the situation when the studied attribute varies across phylogenetic 334 scales without any obvious trend. In this case, the suitable scale of investigation should be defined 335 a priori, based on the objective of the study. The results from one scale will be difficult to 336 extrapolate to other scales.  parameters of frequency distributions, metrics that describe community phylogenetic structure, 365 or measures of niche conservatism (see Table 1). Phylogenetic scale can be defined in terms of 366 clade age, clade size, taxonomic rank, the degree of molecular or phenotypic divergence, etc.,

2003)
evolutionary rates Brownian motion model (Felsenstein 1985), Ornstein-Uhlenbeck model (Hansen 1997) of trait evolution . CC-BY-NC-ND 4.0 International license a certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under The copyright holder for this preprint (which was not this version posted July 27, 2016. ; https://doi.org/10.1101/063560 doi: bioRxiv preprint

PHYLOGENETIC SCALE IN PRACTICE 390
The above overview demonstrates that the consideration of phylogenetic scale varies across 391 fields, both in terms of the approach and the vocabulary. Therefore, it seems of value to find a 392 common language to discuss and study phylogenetic scale across disciplines. There are two 393 general approaches with which phylogenetic scale can be considered in ecological and 394 evolutionary research. One is exploratory, where patterns are identified across a range of 395 phylogenetic scales and then explained in the light of specific events or mechanisms. The other 396 approach relies on testing a priori hypotheses, which are based on mechanisms that presumably 397 take place at a given phylogenetic scale. Both approaches have their strengths and either may be 398 appropriate, depending on the objective of a given study; however, we advocate the hypotheses 399 testing approach for most questions. 400 To study the effects of phylogenetic scale, one can evaluate how a specific attribute of 401 interest (such as diversification rate, niche conservatism, geographic distribution, statistical 402 relationships) changes with phylogenetic scale. These attributes may vary randomly or 403 systematically across the phylogeny, be more prevalent at particular scales, or stay unchanged 404 across a discrete set of mutually nested clades (Box 2). We refer to the latter as a domain of 405 phylogenetic scale which, in analogy to spatial domains (Wiens 1989), corresponds to a segment 406 of phylogeny that reveals homogeneity in the attribute of interest. In this section, we consider 407 conceptual and methodological approaches to explore patterns which are phylogenetic scale-408 dependent. higher taxa may not be appropriate for evaluating the processes of community assembly that 416 typically take place at small phylogenetic scales. To test the hypothesis that competition reduces 417 species coexistence, for example, small phylogenetic scales (e.g. genera, or generally clades where 418 species can reasonably compete) should be preferred to large scales where most species are 419 . CC-BY-NC-ND 4.0 International license a certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under The copyright holder for this preprint (which was not this version posted July 27, 2016. ; https://doi.org/10.1101/063560 doi: bioRxiv preprint highly unlikely to compete (e.g. the entire classes, such as birds and mammals). However, even 420 with a specific question at hand, it can be difficult to choose a single most appropriate 421 phylogenetic scale. Therefore, evaluating multiple phylogenetic extents or grains should be 422 Two potential issues associated with the evaluation of all nodes are data non-451 independence and nestedness. Non-independence can be readily accommodated by the widely 452 used comparative methods (e.g. PIC, PGLS) (Hurlbert 1984;Felsenstein 1985;Freckleton et al. 453 2002;Rohlf 2006). These methods typically estimate the same parameters as their conventional 454 counterparts (e.g. intercepts, regression slopes, group means) but adjust the confidence intervals 455 for these parameters based on the inferred degree of phylogenetic correlation in the data 456 (Hurlbert 1984;Felsenstein 1985;Freckleton et al. 2002;Rohlf 2006). The nestedness of the data is 457 more difficult to accommodate. For example, the diversification rate of a clade is inherently 458 Such discontinuities provide the opportunity to delimit the domains of phylogenetic scale (Box 2). 490 Domains are discrete segments of a phylogeny, such as monophyletic clades, taxonomic ranks, 491 or tree depth, which show homogeneity in the attribute of interest (i.e. diversification rate, 492 statistical correlation, or phylogenetic signal). By definition, the attribute stays largely unchanged 493 within a domain but varies substantially between domains. Phylogenetic domains may therefore 494 provide insights into the processes which operate over different segments of a phylogenetic tree. 495 Traditionally, phylogenetic domains were delimited by taxonomists whose objective was 496 to organize species into biologically meaningful units, such as families, orders, or classes. These 497 units are based mostly on morphological and ecological attributes. However, phylogenetic 498 domains can also consist of clades that show diversification homogeneity, similar rates of 499 morphological evolution, or similar life-history trade-offs. Therefore, the domains may be 500 delimited based on key innovations, episodes of historical dispersals, or extinction events, but 501 also statistically, using quantitative methods without the prior knowledge of the evolutionary 502 history of a clade. While the statistical approach may be more transparent and reproducible, the 503 resulting domains may be harder to interpret biologically. Nonetheless, statistically delimited 504 domains may reveal otherwise unnoticed evolutionary events and potentially important breaks 505 in the clade's history that may have shaped its extant diversity. 506 Phylogenetic domains may further facilitate statistical inference, given that most 507 comparative methods assume that the analyzed attributes are largely homogeneous (e.g. 508 . CC-BY-NC-ND 4.0 International license a certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under The copyright holder for this preprint (which was not this version posted July 27, 2016. ; https://doi.org/10.1101/063560 doi: bioRxiv preprint regression slopes do not vary across genera within the analyzed family, diversification is 509 homogenous across the analyzed lineages) and return spurious results when applied to clades 510 that show a mixture of patterns and processes ( It is well established that different processes dominate over different spatial and temporal scales. 517 Phylogenetic scale, however, has received limited attention although much research in ecology 518 and evolution relies on molecular phylogenies (Table 1). Explicit consideration of phylogenetic 519 scale, scale dependence, phylogenetic scaling, and the domains of phylogenetic scale can 520 therefore inform multiple disciplines in the field (e.g. diversification analysis, community 521 ecology, biogeography and macroecology). 522 We have discussed phylogenetic scale largely in isolation from spatial and temporal 523 scales, but these types of scale will often be related. For instance, competitive exclusion may be 524 prominent among closely related species within local communities over short time periods 525  We hope that the perspective presented here will spur further theoretical, empirical, and 536 methodological research. Explicit consideration of phylogenetic scale may turn our focus away 537 from the importance of particular mechanisms (diversification, trait evolution, niche 538 . CC-BY-NC-ND 4.0 International license a certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under The copyright holder for this preprint (which was not this version posted July 27, 2016. ; https://doi.org/10.1101/063560 doi: bioRxiv preprint conservatism) toward the appreciation for the interplay of multiple processes which together, but 539 over different phylogenetic scales, shape the diversity of life.              CC-BY-NC-ND 4.0 International license a certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under The copyright holder for this preprint (which was not this version posted July 27, 2016. ; https://doi.org/10.1101/063560 doi: bioRxiv preprint