Incipient radiation within the dominant Hawaiian tree Metrosideros polymorpha
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Although trees comprise a primary component of terrestrial species richness, the drivers and temporal scale of divergence in trees remain poorly understood. We examined the landscape-dominant tree, Metrosideros polymorpha, for variation at nine microsatellite loci across 23 populations on young Hawaiâi Island, sampling each of the islandâs five varieties throughout its full geographic range. For four varieties, principal coordinate analysis revealed strong clustering of populations by variety across the 10â430âkm island, indicating partitioning of the species into multiple evolutionarily significant units. The single island-endemic form, riparian var. newellii, showed especially strong differentiation from other varieties despite occurring in sympatry with other varieties and likely evolved from a bog form on the oldest volcano, Kohala, within the past 500â000 years. Along with comparable riparian forms on other Pacific Islands, var. newellii appears to represent parallel incipient ecol...
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2025-04-01
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Collected data represented 423 species from the order Acreodi (1), Artiodactyla (206), Carnivora (178), Cimolesta (4), Condylarthra (3), Hyaenodonta (5), Oxyaenodonta (4), Dinocerata (1), Litopterna (1), Perissodactyla (59) and Procreodi (2) spanning throughout the Cenozoic. On average, data for each species were assembled by merging multiple individual references and for this reason, the collected values were checked for errors. The error checking followed the protocol proposed by (Cooper & Purvis, 2009) to estimate typographical and measurement errors. Ecological data To identify the selective pressures affecting long bones evolution, we collected for both extant and extinct species trophic level, diet, and locomotor behaviour, while only for extant species collected habitat type. The trophic level category was built using body mass as a reference. This category includes: -large predators Extant and extinct Carnivora weighting ≥21.5 kg (Carbone et al., 1999). Examples of fossil genera included in this category were amphicyonids, nimravids, barbourofelids, machairodonts, and arctocyonids. -large prey Extant and extinct Perissodactyla and Artiodactyla including the fossil groups of phenacodontids, merycoidodonts, agriochoerids, and uintatherids weighting from 10 kg up to 900 kg (Estes, 1974). -small predators Small carnivores, weighing less than 21.5 kg (Carbone et al., 1999; Carbone et al., 2007), and feed on small vertebrate and invertebrate food sources. Examples of fossil species included in this category were Desmocyon, Cormocyon, Phlaocyon, and Archaeocyon as well as Eucyon, Limocyon, Thinocyon, Palaeonictis, Buxolestes, Paleosinopa, and Chriacus. -small prey Small ungulates weigh less than 10 kg (Carbone et al., 1999; Carbone et al., 2007). -mega-herbivores Large ungulates weighing more than 900 kg (Sunquist & Sunquist, 1989; Owen‐Smith & Mills, 2008). Among the fossil genera included in this category were Toxodon, Palaeosyops, Parvicornus, Coelodonta, Stephanorhinus, Chilotherium, Teleoceras, Paraceratherium, Amynodon, Chalicotherium, and Moropus. -non-specialized predators This category included species belonging to the family Ursidae which did not show particular predator morphology. Ursids consume less than 10% of ungulates meat (Penteriani & Melletti, 2020). Fossil species belonging to this category were representative of the cave bear group. The only exception was the short-faced bear Arctodus simus which is the largest omnivorous that ever lived (Figueirido et al., 2010; Meloro, 2011; Figueirido et al., 2017). The red panda (Ailurus fulgens) was also included in this category, even though it is not an ursid, as it is well-adapted to a mostly folivorous diet, similar to that of the unrelated giant panda Ailuropoda melanoleuca (Roka et al., 2021). The diet category included: insectivore, carnivorous, omnivore, piscivore, frugivore, folivore, browser, grazer, and mixed feeders. - Insectivores Species feeding on insects such as herpestids, the hyena Proteles, the canid Otocyon, and the extinct genus Hemihegetotherium. - carnivorous Carnivorans feed on vertebrate food, such as most of the Carnivora, Hyaenodonta, Oxyaenodonta, and the genus Pachyaena. - omnivore This category included generalist species such as suids and bears. - piscivore This category included Pantolestidae and otters. - frugivore Species feed mainly on fruits, such as the ring-tailed cat and the genus Bassariscus. - folivores Non-ungulates herbivores as for example the genera Coryphodon, Ailurus, Ailuropoda, and Tremarctos. -browser Ungulates feeding on leaves. Examples of species belonging to this category are Eurygenium, Uintatherium, the basal perissodactyls Hyracotherium, most rhinoceroses, and camelids. -grazer Species feeding on grass as for example the genera Equus, Cervus, Bos, and Bison. -mixed feeders This category included species that feed on both leaves and grass. The extinct Mericoidodontinae that lived before the early Miocene, were classified as browsers, while those that lived from the middle Miocene forward were considered grazers (Mihlbachler & Solounias, 2006). The locomotor behaviour category included amphibious, arboreal, terrestrial, scansorial, and semi-fossorial categories. -arboreal This category included species living on trees. Viverrids, procyonids, small felids, and the genus Miacis are examples of species in this category. -terrestrial This category included most of the carnivoran and ungulate species. -amphibious This category included species living close to bodies of water such as extant polar bears, otters, the hippopotamus, some Tapirus, and the extinct Teleoceras, Buxolestes, Palaeosinopa, and Metamynodon. -scansorial This category included species capable of climbing. Most felids, Mephitidae, Mustelidae, Procyonidae, and the extinct Agriochoerus antiquus and Chriacus were in this category. -semifossorial This category included Meles meles, Mellivora capensis, and Taxidea taxus. For living species only we collected also habitat preferences by merging the IUCN Red List of Threatened Species (www.iucnredlist.org), the primary source, and Animal Diversity Web (animaldiversity.org) information. This category included open, mixed, closed, and wetland habitat types. Phylogenetic tree The phylogenetic position of both living and fossil species and node ages were collected from published articles. These data were used to assemble and calibrate the phylogenetic tree used to take the non-independence of the species into account when computing in the statistical analyses. Time bins In our work entitled "Morphological disparity of mammalian limb bones throughout the Cenozoic: the role of biotic and abiotic factors” we computed morphological disparity of long bones functional indices over the Cenozoic. To bin both species and the estimated ancestral character state according to the Cenozoic stages, we collected the Geological dates from the International Chronostratigraphic Chart 2021 (https://stratigraphy.org/ICSchart/ChronostratChart2021-07.pdf (Cohen et al., 2021). The species first and last appearance in the fossil record were collected from Fossilworks (http://fossilworks.org/), Paleobiology database (https://paleobiodb.org/#/), and Now database (https://nowdatabase.org/). Analyses For the aim of this work, we first investigated the allometric effect studying the relationships between phenotypic traits such as radius to humerus and tibia to femur ratios with the greatest skull length using Phylogenetic Generalised Least Squares regression (PGLS; Harris & Steudel, 1997). The PGLS method incorporates phylogeny as an error term by estimating the lambda parameter, which accounts for different degrees of phylogenetic signal. To determine the functional morphospace taking into account both the effect of the allometry and phylogeny, we computed the size and phylogenetic corrected PCA (Phy-PCA; Revell, 2009). The function phyl.resid (R package phytools; Revell, 2012) was used to remove the allometric effect from the functional ratios, and the function phyl.pca (R package phytools; Revell, 2012) was used to obtain evolutionary-independent Principal Component (PCs). In this study, we also analysed the effect of trophic level, diet, substrate preferences, and habitat on limb proportions using the permutation ANOVA (Collyer & Adams, 2018). In addition, we estimated the ancestral characters at tree nodes to correct morphological disparity computation accounting for sample incompleteness within Cenozoic time bins. The best mode of evolution was assessed for each PC vector using fitContinuous function (R package geiger; Pennell et al., 2014) which allowed testing evolutionary models alternative to Brownian Motion. The Akaike Information Criterion (AIC) was computed to compare the fitted models, with the best models selected based on the lowest AICc and a ΔAIC of less than 2. The best model of evolution for the categorical variables was investigated using fitDiscrete function (R package geiger; Pennell et al., 2014), and selected by comparing AICs and ΔAICs. The best model parameters were used to estimate the ancestral character states for both continuous and discrete variables. Disparity through time, which is a metric that represents morphological variance among species within a specific time interval, was computed by accounting or not for the reconstructed ancestral state. The Partial Disparity Analysis (PDA) was also computed to explore how ecological groups and orders contributed to the changes in morphological disparity. Because our study aimed to investigate the effect of temperature and primary productivity on morphological disparity in mammalian limb proportions throughout the Cenozoic, we collected climatic data from Zachos et al. (2008) and used the linear stochastic differential equation (SDE) approach to test the hypothesis that environmental changes and/or clade interactions affected morphological variation. Finally, we used the swapOne function (R package RRphylo; (Raia et al., 2019) to validate the results in light of phylogenetic uncertainty. References Carbone, C., Mace, G. M., Roberts, S. C., & Macdonald, D. W. (1999). Energetic constraints on the diet of terrestrial carnivores. Nature, 402(6759), 286-288. https://doi.org/10.1038/46266 Carbone, C., Teacher, A., & Rowcliffe, J. M. (2007). The costs of carnivory. PLoS biology, 5(2), e22. https://doi.org/10.1371/journal.pbio.0050022 Cohen, K. M., Finney, S. C., Gibbard, P. L., & Fan, J.-X. (2021). The ICS International Chronostratigraphic Chart. Episodes, 36, 199-204. Collyer, M. L., & Adams, D. C. (2018). RRPP: RRPP: An R package for fitting linear models to high-dimensional data using residual randomization. Methods in Ecology and Evolution, 9(2), 1772-1779. Cooper, N., & Purvis, A. (2009). What factors shape rates of phenotypic evolution? A comparative study of the cranial morphology of four mammalian clades. Journal of Evolutionary Biology, 22(5), 1024–1035. Estes, R. D. (1974). Social organization of the African Bovidae. In V. Geist & E. Walther (Eds.), The behaviour of ungulates and its relation to management (Vol. 1, pp. 166-205),. International Union for Conservation of Nature and Natural Resources. Morges, Switzerland. Figueirido, B., Pérez-Claros, J. A., Torregrosa, V., Martín-Serra, A., & Palmqvist, P. (2010). Demythologizing Arctodus simus, the'short-faced’long-legged and predaceous bear that never was. Journal of Vertebrate Paleontology, 30(1), 262-275. Figueirido, B., Pérez-Ramos, A., Schubert, B. W., Serrano, F., Farrell, A. B., Pastor, F. J., Neves, A. A., & Romero, A. (2017). Dental caries in the fossil record: a window to the evolution of dietary plasticity in an extinct bear. Scientific reports, 7(1), 17813. Harris, M. A., & Steudel, K. (1997). Ecological correlates of hind‐limb length in the Carnivora. Journal of Zoology, 241(2), 381-408. https://doi.org/https://doi.org/10.1111/j.1469-7998.1997.tb01966.x Meloro, C. (2011). Feeding habits of Plio-Pleistocene large carnivores as revealed by the mandibular geometry. Journal of Vertebrate Paleontology, 31(2), 428-446. https://doi.org/https://doi.org/10.1080/02724634.2011.550357 Mihlbachler, M. C., & Solounias, N. (2006). Coevolution of tooth crown height and diet in oreodonts (Merycoidodontidae, Artiodactyla) examined with phylogenetically independent contrasts. Journal of Mammalian Evolution, 13(1), 11-36. https://doi.org/https://doi.org/10.1007/s10914-005-9001-3 Owen‐Smith, N., & Mills, M. G. (2008). Predator–prey size relationships in an African large‐mammal food web. Journal of Animal Ecology, 77(1), 173-183. https://doi.org/10.1111/j.1365-2656.2007.01314.x Pennell, M. W., Eastman, J. M., Slater, G. J., Brown, J. W., Uyeda, J. C., FitzJohn, R. G., Alfaro, M. E., & Harmon, L. J. (2014). geiger v2. 0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees. Bioinformatics, 30(15), 2216-2218. https://doi.org/10.1093/bioinformatics/btu181 Penteriani, V., & Melletti, M. (2020). Bears of the world: Ecology, conservation and management. Cambridge University Press. Raia, P., Castiglione, S., Serio, C., Mondanaro, A., Melchionna, M., & Di Febbraro, M. (2019). RRphylo: Phylogenetic Ridge Regression Methods for Comparative Studies. R package version, 2(0). Revell, L. J. (2009). Size‐correction and principal components for interspecific comparative studies. Evolution: International Journal of Organic Evolution, 63(12), 3258-3268. https://doi.org/10.1111/j.1558-5646.2009.00804.x Revell, L. J. (2012). phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3(2), 217-223. https://doi.org/doi:10.1111/j.2041-210X.2011.00169.x Roka, B., Jha, A. K., & Chhetri, D. R. (2021). A study on plant preferences of red panda (Ailurus fulgens) in the wild habitat: foundation for the conservation of the species. Acta Biologica Sibirica, 7, 425. https://doi.org/ https://doi.org/10.3897/abs.7.e71816 Sunquist, M. E., & Sunquist, F. C. (1989). Ecological constraints on predation by large felids. In J. L. Gittleman (Ed.), Carnivore behavior, ecology, and evolution (pp. 283-301). Springer, Boston, MA. https://doi.org/https://doi.org/10.1007/978-1-4757-4716-4_11 Zachos, J. C., Dickens, G. R., & Zeebe, R. E. (2008). An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics. Nature, 451(7176), 279-283. https://doi.org/10.1038/nature06588
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