Supplementary Material for Dietary innovations spurred the diversification of ruminants during the Cenozoic
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1 Cantalapiedra et al. Suppl. Mat. 1 Supplementary Material for Dietary innovations spurred the diversification of ruminants during the Cenozoic Juan L. CANTALAPIEDRA, Richard G. FITZJOHN, Tyler S. KUHN, Manuel HERNÁNDEZ FERNÁNDEZ, Daniel DEMIGUEL, Beatriz AZANZA, Jorge MORALES and Arne Ø. MOOERS 1. Feeding modes. We followed Hofmann and Stewart s categorization [1] and performed an extensive review of the ecological literature (Table S1 and Sources) in order to assign ruminant species to each of the three broad dietary categories: browsers feed primarily on herbaceous and woody material such as forbs, leaves and fruits; mixed feeders have a composite diet of grasses, rushes and sedges, and browse; grazers concentrate feeding on grasses, rushes and sedges. Table S1. The dietary classification of the 197 ruminant species including extant species and those that became extinct in historical times ( ) is shown according to Hofmann and Stewart s categorization [1] and based on published data. B, browsers, M, mixed feeders, G, grazers. Sources are given in full below. FAMILY SPECIES DIET Tragulidae Hyemoschus aquaticus B Tragulidae Moschiola meminna B Tragulidae Tragulus javanicus B Tragulidae Tragulus napu B Antilocaprinae Antilocapra americana B Giraffidae Giraffa camelopardalis B Giraffidae Okapia johnstoni B Moschidae Moschus moschiferus B Moschidae Moschus berezovskii B Moschidae Moschus chrysogaster B Moschidae Moschus fuscus B Moschidae Moschus cupreus B Moschidae Moschus leucogaster B Cervidae Hydropotes inermis B Cervidae Axis axis M Cervidae Hyelaphus porcinus M Cervidae Hyelaphus calamianensis M Cervidae Hyelaphus kuhlii M Cervidae Dama dama M Cervidae Dama mesopotamica M Cervidae Elaphurus davidianus G Cervidae Rusa alfredi M Cervidae Rusa mariannus M Cervidae Rusa timorensis M Cervidae Rusa unicolor M Cervidae Rucervus duvaucelii M Cervidae Rucervus eldii M Cervidae Rucervus schomburgki M Cervidae Przewalskium albirostris M Cervidae Cervus elaphus M
2 Cantalapiedra et al. Suppl. Mat. 2 FAMILY SPECIES DIET Cervidae Cervus nippon M Cervidae Elaphodus cephalophus B Cervidae Muntiacus atherodes M Cervidae Muntiacus reevesi M Cervidae Muntiacus rooselvetorum M Cervidae Muntiacus truongsonensis M Cervidae Muntiacus putaoensis M Cervidae Megamuntiacus vuquangensis M Cervidae Muntiacus feae M Cervidae Muntiacus muntjak M Cervidae Muntiacus crinifrons M Cervidae Muntiacus gongshanensis M Cervidae Alces alces B Cervidae Capreolus capreolus B Cervidae Capreolus pygargus B Cervidae Rangifer tarandus M Cervidae Blastocerus dichotomus M Cervidae Ozotoceros bezoarticus G Cervidae Odocoileus hemionus B Cervidae Odocoileus virginianus B Cervidae Mazama americana B Cervidae Mazama gouazoupira B Cervidae Mazama chunyi B Cervidae Mazama nana B Cervidae Mazama bricenii B Cervidae Mazama rufina B Cervidae Pudu mephistophiles B Cervidae Pudu puda M Cervidae Hippocamelus antisensis M Cervidae Hippocamelus bisulcus M Bovidae Boselaphus tragocamelus M Bovidae Tetracerus quadricornis M Bovidae Pseudoryx nghetinhensis B Bovidae Bos grunniens G Bovidae Bison bison G Bovidae Bison bonasus M Bovidae Bos sauveli G Bovidae Bos taurus G Bovidae Bos frontalis M Bovidae Bos javanicus M Bovidae Syncerus caffer M Bovidae Bubalus bubalis G Bovidae Bubalus mindorensis M Bovidae Bubalus depressicornis M Bovidae Bubalus quarlesi M Bovidae Taurotragus derbianus M Bovidae Taurotragus oryx M Bovidae Tragelaphus strepsiceros B Bovidae Tragelaphus buxtoni M Bovidae Tragelaphus eurycerus M Bovidae Tragelaphus scriptus M Bovidae Tragelaphus spekii M Bovidae Tragelaphus angasii M Bovidae Tragelaphus imberbis M Bovidae Oreotragus oreotragus B Bovidae Neotragus pygmaeus B Bovidae Neotragus batesi B
3 Cantalapiedra et al. Suppl. Mat. 3 FAMILY SPECIES DIET Bovidae Neotragus moschatus B Bovidae Ourebia ourebi M Bovidae Saiga tatarica M Bovidae Litocranius walleri B Bovidae Ammodorcas clarkei B Bovidae Antidorcas marsupialis M Bovidae Antilope cervicapra G Bovidae Eudorcas rufina M Bovidae Eudorcas rufifrons M Bovidae Eudorcas thomsonii M Bovidae Nanger granti B Bovidae Nanger dama M Bovidae Nanger soemmerringii B Bovidae Gazella bennettii M Bovidae Gazella spekei M Bovidae Gazella bilkis M Bovidae Gazella arabica M Bovidae Gazella gazella M Bovidae Gazella saudiya M Bovidae Gazella dorcas M Bovidae Gazella cuvieri M Bovidae Gazella subgutturosa M Bovidae Gazella leptoceros M Bovidae Procapra gutturosa M Bovidae Procapra picticaudata M Bovidae Procapra przewalskii M Bovidae Madoqua guentheri B Bovidae Madoqua kirkii B Bovidae Madoqua piacentinii B Bovidae Madoqua saltiana B Bovidae Dorcatragus megalotis M Bovidae Raphicerus campestris B Bovidae Raphicerus melanotis M Bovidae Raphicerus sharpei M Bovidae Sylvicapra grimmia B Bovidae Cephalophus adersi B Bovidae Cephalophus niger B Bovidae Cephalophus rubidus B Bovidae Cephalophus callipygus B Bovidae Cephalophus weynsi B Bovidae Cephalophus leucogaster B Bovidae Cephalophus harveyi B Bovidae Cephalophus natalensis B Bovidae Cephalophus rufilatus B Bovidae Cephalophus nigrifrons B Bovidae Cephalophus jentinki B Bovidae Cephalophus dorsalis B Bovidae Cephalophus silvicultor B Bovidae Cephalophus spadix B Bovidae Cephalophus ogilbyi B Bovidae Cephalophus zebra B Bovidae Philantomba maxwellii B Bovidae Philantomba monticola B Bovidae Pelea capreolus B Bovidae Redunca fulvorufula G Bovidae Redunca arundinum G Bovidae Redunca redunca G
4 Cantalapiedra et al. Suppl. Mat. 4 FAMILY SPECIES DIET Bovidae Kobus kob G Bovidae Kobus vardonii G Bovidae Kobus ellipsiprymnus G Bovidae Kobus leche G Bovidae Kobus megaceros M Bovidae Aepyceros melampus M Bovidae Alcelaphus buselaphus G Bovidae Sigmoceros lichtensteinii G Bovidae Connochaetes gnou G Bovidae Connochaetes taurinus G Bovidae Beatragus hunteri G Bovidae Damaliscus lunatus G Bovidae Damaliscus pygargus G Bovidae Addax nasomaculatus M Bovidae Oryx dammah M Bovidae Oryx gazella M Bovidae Oryx leucoryx M Bovidae Hippotragus niger G Bovidae Hippotragus equinus G Bovidae Hippotragus leucophaeus G Bovidae Pantholops hodgsonii M Bovidae Budorcas taxicolor M Bovidae Ovibos moschatus M Bovidae Ammotragus lervia M Bovidae Capra falconeri M Bovidae Capra hircus M Bovidae Capra caucasica M Bovidae Capra cylindricornis M Bovidae Capra pyrenaica M Bovidae Capra ibex M Bovidae Capra nubiana M Bovidae Capra sibirica M Bovidae Capra walie M Bovidae Hemitragus jemlahicus M Bovidae Hemitragus hylocrius M Bovidae Hemitragus jayakari M Bovidae Pseudois nayaur M Bovidae Pseudois schaeferi M Bovidae Ovis ammon G Bovidae Ovis aries G Bovidae Ovis vignei M Bovidae Ovis nivicola M Bovidae Ovis canadensis M Bovidae Ovis dalli M Bovidae Oreamnos americanus M Bovidae Rupicapra pyrenaica M Bovidae Rupicapra rupicapra M Bovidae Naemorhedus baileyi M Bovidae Naemorhedus caudatus M Bovidae Naemorhedus goral M Bovidae Capricornis sumatraensis M Bovidae Capricornis crispus M Bovidae Capricornis swinhoei M
5 Cantalapiedra et al. Suppl. Mat. 5 Feeding Mode Sources Barrette C Antler eating and antler growth in wild Axis deer. Mammalia 49, Barrette C The comparative behaviour and ecology of chevrotains, musk deer, and morphologically conservative deer. In Biology and Management of the Cervidae (ed. Wemmer C M), pp Washington, DC, Smithsonian Institution. Bell RHV A grazing system in the Serengeti. Sci. Am. 224, Bergerund AT Food habits of the Newfoundland caribou. J. Wildl. Manag. 36, Bodmer RE Ungulate biomas in relation to feeding strategy within Amazonian forest. Oecologia 81, Bodmer RE Ungulate frugivores and the browser-grazer continuum. Oikos 57, Branan WV, Wekhoven MC, Marchinton RL Food habits of brocket and whitetailed deer in Suriname. J. Wildl. Manag. 49, Bugalho MN, Milne JA, Racey PA The foraging ecology of red deer (Cervus elaphus) in a Mediterranean environment: is a larger body size advantageous? J. Zool. 255, Bullock DJ Annual diets of hill sheep and feral goats in southern Scotland. J. Appl. Ecol. 22, Campos-Arceiz A, Takatsuki S Food habits of sika deer in the Shiranuka Hills, eastern Hokkaido: a northern example from the north south variations in food habits in sika deer. Ecol. Res. 20, (doi: /s ). Chapman JA, Feldhammer GA Wild mammals of North America: Biology, Management, and Conservation. Baltimore, The Johns Hopkins Univiversity Press; 1232 p. Du Toit JT Feeding-height stratification among African browsing ruminants. Afr. J. Ecol. 28, (doi: /j tb01136.x).
6 Cantalapiedra et al. Suppl. Mat. 6 Estes RD The Behavior Guide to African Mammals: Including Hoofed Mammals, Carnivores, Primates. Berkeley and Los Angeles, California, University of California Press. Geist V Mountain Sheep: a Study in Behavior and Evolution. Chicago, University of Chicago Press. Geist V Deer of the World: Their Evolution, Behaviour, and Ecology. Mechanisburg, PA, Stackpole Books; 428 p. Gordon IJ, Illius AW The nutritional ecology of African ruminants: a reinterpretation. J. Anim. Ecol. 65, Hansen RM, Clark RC Foods of elk and other ungulates at low elevations in northwestern Colorado. J. Wildl. Manag. 41, Hoefs M Food selection by Dall's sheep (Ovis dalli dalli Nelson). In The Behaviour of Ungulates and its Relation to Management (eds. Geist V, Walther F), pp Switzerland, IUCN Publications new series, Morges. Hofmann RR Ruminant Stomach: stomach structure and feeding habits of eastern African game ruminants. Nairobi, East African Literature Bureau; 354 p. Hofmann RR Digestive physiology of the deer-their morphophysiological specialization and adaptation. R. Soc. New Zealand Bull. 22, Hofmann RR Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system. Oecologia 78, Homolka M Foraging strategy of large herbivores in forest habitats. Folia Zool. 45, Illius AW, Gordon IJ The physiological ecology of mammalian herbivores. In Nutritional Ecology of Herbivores (eds. Jung H J G, Fahey G C), pp Savoy, Ill, American Society of Animal Science. Janis CM An estimation of tooth volume and hypsodonty indices in ungulate mammals, and the correlation of these factors with dietary preference. In Teeth Revisited: Proceedings of the VII International Symposium on Dental Morphology (eds. Russell D, Santoro J, Sigogneau-Russell D), pp París.
7 Cantalapiedra et al. Suppl. Mat. 7 Kingdon J East African Mammals: An Atlas of Evolution in Africa, Volume 3, Part D:Bovids. Chicago, University of Chicago Press. Labaô-Tello J, Van Gelder RJ The natural history of the nyala (Tragelaphus angasi) (Mammalia Bovidae). Bull. Am. Mus. Nat. Hist. 155, Laca EA, Demment MW Foraging strategies of grazing animals. In The Ecology and Management of Grazing Systems (eds. Hodgson J, Illius A W), pp Wallingford, CAB International. Liu B, Jiang Z Foraging strategy of Przewalski's gazelle. Acta Zool. Sin. 48, Lu CD Grazing behavior and diet selection of goats. Small Ruminant Res. 1, Lumpkin S, R. KK Cephalophus sylvicultor. Mamm. Sp. 225, 1-7. McDonald JN North American Bison: their classification and evoltion. Berkeley, University of California Press. McNaughton SJ, Georgiadis NJ Ecology of African grazing and browsing mammals. Annu. Rev. Ecol. Syst. 17, Milne JA Diet selection by grazing animals. Proc. Nutr. Soc. 50, Nowak RM Walker s mammals of the world. 4th ed ed. Baltimore, MD, The Johns Hopkins Univiversity Press; 2015 p. Nudds TD Forage "preference": theoretical consideration of diet selection by deer. J. Wildl. Manag. 44, O Gara BW, Yoakum JD Pronghorn ecology and management. Boulder, University Press of Colorado; 903 p. Papachristou TG, Dziba LE, Provenza FD Foraging ecology of goats and sheep on wooded rangelands. Small Ruminant Res. 59, (doi: /j.smallrumres ). Pérez-Barbería FJ, Gordon IJ The influence of sexual dimorphism in body size and mouth morphology on diet selection and sexual segregation in cervids. Acta Vet. Hung. 46,
8 Cantalapiedra et al. Suppl. Mat. 8 Pérez-Barbería FJ, Gordon IJ, Nores C Evolutionary transitions among feeding styles and habitats in ungulates. Evol. Ecol. Res. 3, Schaller G, Qitao T, Wenshi P, Zisheng HJ, Heming S Feeding behavior of Sichuan takin (Budorcas taxicolor). Mammalia 50, (doi: /mamm ). Schaller GB The Deer and the Tiger. Chicago, University Chicago Press; 384 p. Schaller GB Distribution. In Mountain Monarchs: Wild Sheep and Goats of the Himalaya. (ed. Schaller G B), pp Chicago, University of Chicago Press. Seligman NG Management of Mediterranean Grasslands. In The Ecology and Management of Grazing Systems (eds. Hodgson J, Illius A W), pp , CAB International. Sheng HL The Deer in China. Shanghai, East China Normal University Press. Sinclair ARE The African buffalo: a study of resource limitation of populations. Chicago University Chicago Press. Stronge DC, Fordham RA, Minot EO The foragins ecology of feral goats Capra hircus in the Mahoenui Giant Weta Reserve, southern King Country, New Zeland. N. Z. J. Ecol. 21, Tener JS Muskoxen in Canada: a biological and taxonomic review. Ottawa (Canada), Canadian Wildlife Service. Van Soest PJ Nutritional Eecology of the Ruminant. 2nd ed. Ithaca, New York, Comstock Publishing. 2. Polytomies resolution and phylogenetic uncertainty. Polytomies in the ruminants supertree [2] are soft representing missing data rather than true multifurcations and would bias almost any statistic that draws on tree shape, as we do here. We therefore resolved polytomies using node constraints and a birth-death prior in BEAST [3, 4], with an additional modification allowing for specification of individual priors on every node, whether fully resolved or polytomous. Where only molecular dates were available, calibration used a normal prior, with mean equal to the median of the molecular calibrations and the standard deviation equal to the (maximum age
9 Cantalapiedra et al. Suppl. Mat. 9 minimum age)/1.96. For nodes with both molecular and fossil dates, only those molecular dates older than the fossil date were included in the calibration. For these nodes, calibrations used a truncated normal prior with the fossil age providing a minimum bound and with the mean and standard deviation estimated as before. If only fossil dates were available, calibration again used a truncated normal prior. Here we fitted a linear regression model to the log-transformed molecular and fossil dates for all nodes with both types of dates. The molecular dates were scaled as a proportion of the fossil age (molecular date / fossil date) to account for increased variance in older dates. Using separate regression models for median molecular age and maximum molecular age, we inferred the missing mean and standard deviation for the normal prior of each node. The remaining 20% of the nodes used no calibrations, allowing the node age to be interpolated from the tree-wide birth-death model parameters [3]. This prior model should be unbiased with respect to our analyses of feeding mode, and offer only noise with respect to time-based analyses. Using BEAST v1.6.2 [4], we ran the polytomy resolution for 11,100,000 generations, sampling every 1,000 generations, with the first 10% discarded as a burnin. From the resulting 10k tree distribution, we randomly sampled 100 trees for use in further analyses (a lineage-through time plot for the 100 trees is shown in Main text figure 1b). 3. Testing the power of MuSSE to detect climate dependent trends. We tested whether the speciation rates are associated with climate by adding a paleoclimate proxy [5] to our models. As this is a new analysis, to ensure that our difference in model fit was robust, we used simulations to determine MuSSE s ability to recover the influence of climate. Because the power to detect state-dependent diversification has been explored elsewhere [6-8], we focus on the power to detect the correlation with a timevarying proxy. As detailed in the Methods section, we parameterized the speciation rate as a function of climate through time as λ i ( t) = λ 0i + ( λ 1i λ 0i ) δ 18 O where λ i (t) is the speciation rate over time for state i, δ 18 O is the smoothed and scaled δ 18 O function (lower values for higher temperature), and λ 0i and λ 1i are the speciation
10 Cantalapiedra et al. Suppl. Mat. 10 rates corresponding to the minimum and maximum values of δ 18 O. Where λ 0i = λ 1i, this reduces to the time-constant MuSSE model (i.e., λ i (t) = λ 0i ). For our simulations, we configured different sets of parameters. We held λ 0i + λ 1i at 0.1 and simulated trees where the ratio between λ 0i and λ 1i was {0.125, 0.25, 0.5, 1, 2, 4, 8}. When below 1 λ 0i is lower than λ 1i the scale parameter indicates a decreasing speciation rate with temperature and time and when above 1 λ 0i is higher than λ 1i it indicates increasing speciation rate with temperature or time. Note that δ 18 O and temperature correlate inversely. When this ratio is equal to 1, it reduces to the constant model (flat line in figure S1). Figure S1. Representation of δ 18 O-dependent speciation rates profiles. The ratio between λ0i and λ 1i can be below 1 (higher speciation with lower temperatures; blue lines) or above 1 (higher speciation with higher temperatures; red lines). For each of the seven parameter sets, we simulated 500 trees over 55 myr using the TESS package [9] in R [10]. We the looked at the proportion of trees where the climatedependent birth-death fit represents an improvement over a constant rate birth-death model assessed with a likelihood ratio test with 1 d.f.. The result is represented in figure S2, where the power of capturing the climate effect and the size of the trees has been plotted and fitted using a logistic regression. Overall, the power to detect the effect of climate increases with the size of the tree (figure S2). For a given tree size, there was more power to detect a generally decreasing speciation rate over time (red lines in figure S1 and S2) than an increasing speciation rate over time (blue lines). For example, for trees with around 200 species, such as the ruminant tree we use, the method has good power to detect small effects if they exist. However, if there is a pattern of generally increasing speciation rates with time the method may miss even strong effects.
11 Cantalapiedra et al. Suppl. Mat. 11 Figure S2. The proportion of trees for which a climate-dependent birth-death model represents an improvement over the constant rate model is plotted against the number of species of the simulated trees. 4. Evolutionary models with speciation and extinction independent of diet. We here show the comparison of the six models described in the main text (MuSSE and MuSSE+climate) with three extra MuSSE models where speciation (λ) and extinction (µ) rates were fixed to be equal across all feeding behaviours. MuSSE+climate models P Mean ΔAIC flexible+climate unconstrained+climate towards-grazing+climate MuSSE flexible unconstrained towards-grazing λ and µ constrained equal across diets flexible.constrained unconstrained.constrained towards-grazing.constrained Table S2. Model fitting (ΔAIC) including three extra models where speciation rates (λ) are forced to be equal. Under each category (climatic, plain MuSSE and constrained models), models are ordered by mean ΔAIC rank. The number of parameters in each model is given (P).
12 Cantalapiedra et al. Suppl. Mat Additional References 1. Hofmann RR, Stewart DRM Grazer or Browser: a classification based on the stomach structure and feeding habits of East African ruminants. Mammalia 36, Hernández Fernández M, Vrba ES A complete estimate of the phylogenetic relationships in Ruminantia: a dated species-level supertree of the extant ruminants. Biol. Rev. 80, (doi: /s ). 3. Kuhn TS, Mooers AØ, Thomas GH A simple polytomy resolver for dated phylogenies. Meth. Ecol. Evol. 2, (doi: /j x x). 4. Drummond AJ, Rambaut A BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 1-8. (doi: / ). 5. Zachos J, Pagani M, Sloan L, Thomas E, Billups K Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 293, (doi: /science ). 6. Maddison WP, Midford PE, Otto SP Estimating a binary character's effect on speciation and extinction. Syst. Biol. 56, (doi: / ). 7. FitzJohn RG diversitree: comparative phylogenetic tests of diversification in R. Meth. Ecol. Evol. 3, (doi: /j x x). 8. FitzJohn RG, Maddison WP, Otto SP Estimating trait-dependent speciation and extinction rates from incompletely resolved phylogenies. Syst. Biol. 58, (doi: /sysbio/syp067). 9. Höhna S Fast simulation of reconstructed phylogenies under global, timedependent birth-death processes. Bioinformatics 29, (doi: /bioinformatics/btt153).
13 Cantalapiedra et al. Suppl. Mat R Development Core team R: A language and environment for statistical computing. (Viena, Austria. ISBN , URL R Foundation for Statistical Computing.
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