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Morphological variation in the genus Chlorocebus: Ecogeographic and anthropogenically mediated variation in body mass, postcranial morphology, and growth
Trudy R. Turner University of Wisconsin - Milwaukee
Christopher A. Schmitt Boston University
Jennifer Danzy Cramer American Military University
Joseph Lorenz Central Washington University
J. Paul Grobler University of the Free State
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Recommended Citation Turner, TR, Schmitt, CA, Cramer, JD, et al. Morphological variation in the genus Chlorocebus: Ecogeographic and anthropogenically mediated variation in body mass, postcranial morphology, and growth. Am J Phys Anthropol. 2018; 166: 682– 707. https://doi.org/10.1002/ajpa.23459
This Article is brought to you for free and open access by the College of the Sciences at ScholarWorks@CWU. It has been accepted for inclusion in All Faculty Scholarship for the College of the Sciences by an authorized administrator of ScholarWorks@CWU. For more information, please contact [email protected]. Authors Trudy R. Turner, Christopher A. Schmitt, Jennifer Danzy Cramer, Joseph Lorenz, J. Paul Grobler, Clifford J. Jolly, and Nelson B. Freimer
This article is available at ScholarWorks@CWU: https://digitalcommons.cwu.edu/cotsfac/332
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Ellensburg, WA 98926, USA USA WA 98926, Ellensburg, anthropogenically mediated variation in body mass, postcranial morphology, and postcranial body mass, in variation mediated anthropogenically J. Paul Grobler Paul J. Trudy R. Turner Trudy R. growth Clifford J. Jolly Clifford J.
Morphological variation in the genus genus the in variation Morphological 6 5 4 3 2 1 Jennifer Danzy Cramer Jennifer Nelson B. Freimer B. Nelson University and American Public University, Charles Town, WV 25414, USA USA Charles WV 25414, Town, University, Public American and University CA USA 90095, Angeles, USA 53201, Christopher A. Schmitt A. Christopher Joseph Lorenz Joseph Author University, Washington Central Studies, of Anthropology Museum and Department Military American Studies, Women's and of Sociology, Anthropology Department Los Angeles, Los – University of California Genetics, for Neurobehavioral Center 02215, MA USA Boston, University, Boston of Anthropology, Department Africa South FS, Bloemfontein, Free State, of the University of Genetics, Department Manuscript WI Milwaukee, Milwaukee, – of Wisconsin University of Anthropology, Department 7 6 2
1,2* 4
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American JournalofPhysicalAnthropology
Chlorocebus : Ecogeographic and and : Ecogeographic 1
ABBREVIATED TITLE: ABBREVIATED ABSTRACT ABSTRACT Milwaukee. Sabin Hall, Room 125B. PO Box 413. Milwaukee, WI 53201. Email: Email: WI 53201. Milwaukee, Box PO 413. Room 125B. Hall, Sabin Milwaukee.
KEY WORDS: KEY 7 Trudy R. Turner, Department of Anthropology, University of Wisconsin – – of Wisconsin University of Anthropology, Department Turner, Trudy R. AUTHOR: *CORRESPONDING Text pages (plus bibliography), 50 pages. Figures, 6. Tables, 8. Tables, 6. Figures, 50 pages. bibliography), (plus pages Text USA 10003, NY Samples were collected through funding from NIH grants R01RR016300 and and R01RR016300 grants NIH funding from through collected were Samples SPONSORSHIP: GRANT [email protected] variation in patterns of growth and sexual dimorphism. We investigated population population investigated We dimorphism. of growth patterns sexual and in variation R01OD010980 to NBF and NSF grant BN770-3322 to CJJ and TRT. TRT. and CJJ to BN770-3322 grant NSF and NBF to R01OD010980 ecogeographic variation, plastic local variation in response to human impacts, and and impacts, human to response in variation local plastic variation, ecogeographic dispersed wild primate taxa is rarely accomplished, yet critical to understanding understanding to critical yet rarely accomplished, is taxa wild primate dispersed Objectives Author Manuscript York, New NYCEP, and University, of York New Anthropology, Department CSHO, : Direct comparative work in morphology and growth on widely widely on growth and work morphology in comparative : Direct Chlorocebus This article isprotected by copyright. All rights reserved. Comparative growth and morphology of Chlorocebus morphology growth and Comparative American JournalofPhysicalAnthropology , vervet, growth, life history, sexual dimorphism dimorphism sexual history, growth, life vervet, , John Wiley&Sons, Inc.
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Morphological variation in widespread taxa may arise by a number of mechanisms: mechanisms: of number a by may arise taxa widespread in variation Morphological INTRODUCTION patterns will require further comparative work in vervets. vervets. in work further will comparative require patterns Conclusions predicted ways to human impacts. To better understand deviations from predicted predicted from deviations understand To better impacts. human ways to predicted areas were lighter; human impacts had no effect on males. males. on effect had no impacts lighter; were human areas natural selection, developmental plasticity in response to local environmental environmental local to response in plasticity developmental selection, natural by Bergmann’s and, less consistently, Allen’s Rule, while also responding in in responding also while Rule, Allen’s consistently, less and, Bergmann’s by heavier than those with moderate exposures, while those in low human impact low impact human in those while exposures, moderate with those than heavier segments in support for Allen’s Rule. Females in high human impact areas were were areas in impact high human Females for Rule. Allen’s support in segments Bergmann’s Rule in adult females, and in adult males when excluding the St. Kitts & & Kitts St. excluding when the adult males in and females, adult in Rule Bergmann’s the Caribbean, and compared measurements of body mass, body length, and relative relative and body length, of body mass, measurements compared and Caribbean, the least dimorphic. There was significant, although very small, variation in all limb limb all in although variation very small, significant, was There dimorphic. least Methods although the South African population had the largest average body size, it was the the was it size, body had average the largest population African South although the impacts in the vervet monkey ( the in impacts Results Nevis. & Kitts and Africa, St. South Kenya, Nevis population, which was more sexually dimorphic. Contrary to Rensch’s Rule, Rule, Rensch’s Contrary to which dimorphic. sexually more was population, Nevis latitude, altitude), climatic variables (i.e., temperature and rainfall), and human human and rainfall), temperature and (i.e., climatic variables altitude), latitude, thigh, leg, and foot length in four well-represented geographic samples: Ethiopia, Ethiopia, samples: geographic four in well-represented length foot and leg, thigh, variation in morphology and growth in response to geographic variables (i.e., (i.e., variables geographic to response in growth and morphology in variation : We found significant variation in body mass and length consistent with with consistent length and body mass in variation : found We significant Author Manuscript Africa and Sub-Saharan across from overwild vervets : trapped 1600 We : Vervet monkeys appear to have adapted to local climate as predicted predicted as climate local to adapted have to appear monkeys : Vervet This article isprotected by copyright. All rights reserved. American JournalofPhysicalAnthropology Chlorocebus John Wiley&Sons, Inc. spp.). spp.). 3
1989; mandrills: Setchell et al., 2001). Finally, comparisons of morphological of morphological comparisons 2001). Finally, al., et Setchell 1989; mandrills: and Kessler, 1989; mangabeys: Deputte, 1992; baboons: Coelho and Rutenberg, Rutenberg, and Coelho 1992;baboons: Deputte, 1989; mangabeys: Kessler, and (e.g., rhesus macaques: Tanner et al., 1990; Schwartz and Kemnitz, 1992; Turnquist Turnquist 1992; 1990; al., Kemnitz, Schwartz and et macaques: Tanner rhesus (e.g., and Sauther, 2006) or are housed in laboratories or semi-naturalistic environments environments or semi-naturalistic laboratories housed in 2006) are or Sauther, and et al., 2007; Elton et al. 2010). Data on morphological variation are also often often also are variation morphological on Data al. 2007;2010). et al., Elton et Stallmann, 2005; Gombe chimpanzees: Pusey et al., 2005; ring tailed lemurs: Cuozzo 2005; Cuozzo lemurs: al., ring tailed et Pusey chimpanzees: 2005; Gombe Stallmann, used (e.g., Fooden, 1979; Groves, 2001; Kingdon, 2013; Albrecht et al., 1990; 2013; al., Cardini et Albrecht 2001; 1979; Kingdon, Fooden, Groves, used (e.g., often have limited geographic distributions (e.g., booted macaques: Schillaci and and Schillaci macaques: booted (e.g., distributions geographic limited have often number of animals can often be substantial, especially if multiple collections are are collections multiple if especially substantial, be often can of animals number collected from populations of living animals at a single location. Such populations populations Such location. single a at of animals living fromcollected populations number of skins and skeletonized specimens, although the geographic range and and range although geographic the specimens, skeletonized and of skins number collected in primates. Museum specimens can provide information from a limited limited a from provide can information Museum specimens primates. in collected range are crucial to understanding population differentiation, they are they rarely differentiation, population understanding to crucial are range 2011; Lomolino et al. 2006). 2006). al. et 2011; Lomolino become fixed by natural selection (Kuzawa and Bragg, 2012; Kuzawa and Thayer, Thayer, and Kuzawa 2012; Bragg, (Kuzawa and selection fixed natural by become comprised of multiple environmentally driven phenotypes that may ultimately may ultimately that phenotypes driven environmentally of multiple comprised et al. 2007; Roseman & Auerbach, 2015), as well as geographically distinct taxa taxa distinct geographically well as as 2015), Auerbach, 2007; & al. et Roseman substructuring can result in morphological clines within a single taxon (e.g., Cardini Cardini taxon (e.g., single a within clines morphological in result can substructuring In populations with significant amounts of gene flow, local polytypy and and polytypy local flow, of gene amounts significant with In populations used to indicate the possible beginnings of speciation (Hill, 1966; Kingdon, 1997). 1966; (Hill, Kingdon, of speciation beginnings possible the indicate used to variation in subpopulations of taxa with wide distributions has historically been historically has been wide distributions with of taxa subpopulations in variation forces, and random processes like genetic drift. Locally differentiable morphological morphological Locally differentiable drift. genetic like random processes and forces,
Author Manuscript throughout taxon’s a habitats diverse in living fromdata animals Although This article isprotected by copyright. All rights reserved. American JournalofPhysicalAnthropology John Wiley&Sons, Inc. 4 Page 4of69
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response to the selective challenges of differing environments. environments. of differing challenges selective the to response immature mammals, the contribution of developmental patterns to adult to patterns of developmental contribution the mammals, immature understanding of the life history trade-offs that may underlie adult variation in in variation adult may underlie that history trade-offs life of the understanding phenotypes has been critical to understanding adult selective regimes (e.g., Ozgul et (e.g., regimes selective adult understanding to critical been has phenotypes available for adult animals of a particular taxon, it is rare to also have comparable comparable have also to rare is it taxon, particular of a for adult animals available al., 2010; Ozgul et al., 2009). Information on animals of various life stages within and and within stages of various life animals on 2009). Information al., 2010; et al., Ozgul information on multiple life stages. Where comparable data have been on collected been have data comparable Where stages. life multiple on information across closely related but widely dispersed populations is necessary for a complete necessary for is complete a populations dispersed widely but closely related across 1997; Whitten & Turner, 2004). 2004). Turner, & 1997; Whitten multiple locations within a taxon’s range and collected by the same researchers researchers same the by collected and range taxon’s a within locations multiple using comparable protocols (e.g., macaques: Albrecht, 1980; vervets: Turner et al., al., et Turner 1980;vervets: Albrecht, macaques: (e.g., protocols comparable using 2007), Kojima Island in Japan (Hamada et al., 1986) and Polonnaruwa (Cheverud et et (Cheverud 1986) al., (Hamada et Polonnaruwa and Japan Island in Kojima 2007), al., 1992). Only rarely is information available from free ranging animals living in in living animals from ranging free available information 1992). is Only rarely al., data are also available for populations of macaques from Singapore (Schillaci et al., al., et (Schillaci from Singapore of macaques for populations available also are data variation more broadly within genera may be made across numerous independent independent numerous across made may be genera within broadly more variation in the Awash Park, Ethiopia; Altmann and colleagues on baboons in Amboseli in baboons on colleagues and Altmann Ethiopia; Awash Park, the in 1989) and Johnson (2003) on animals from Botswana. Comparative morphological Comparative Botswana. from animals (2003) on Johnson 1989) and example, may be based on the work of Jolly and Phillips-Conroy (2003) on baboons baboons on (2003) Phillips-Conroy work and the based on of Jolly may be example, colleagues on baboons in the Rift Valley area of Kenya (Strum, 1991; Eley et al., al., et 1991; Eley (Strum, Kenya of Valley area Rift the in baboons on colleagues study sites, collected by different research groups. Comparison across baboons, for across baboons, Comparison groups. research different by collected study sites, National Park, Kenya (Altmann et al., 1981; Altmann et al., 1993); Strum and 1993); and al., et Strum 1981; al., Altmann et (Altmann Kenya Park, National
Author are data widespread where geographically cases these in Furthermore, Manuscript This article isprotected by copyright. All rights reserved. American JournalofPhysicalAnthropology John Wiley&Sons, Inc. 5
Ch. pygerythrus hilgerti pygerythrus of Ch. Ch. sabaeus Ch. African first Africa, West diverging into East/Central in Ch. aethiops aethiops of Ch. divergence and isolation the followed by expansion from East Africa around ~265 kya (comprised of the ancestral population population ancestral of the kya (comprised Africa around ~265 from East expansion Vervets are found throughout sub-Saharan Africa. The genus most likely originated likely originated most The genus Africa. sub-Saharan found are throughout Vervets and water, especially in savanna-woodland and open country with riverine forest. forest. country riverine with open and in savanna-woodland especially water, and hot and arid areas, as well as more temperate and cooler areas where winter winter and where areas cooler temperate more well as as arid areas, and hot variety of tropical and subtropical, seasonal habitats that provide sufficient trees trees that sufficient provide habitats seasonal subtropical, and ofvariety tropical The study reported here relies on morphological measurements obtained obtained measurements morphological on relies here reported study The nighttime temperatures may fall below freezing (e.g., Lubbe et al. 2014; Kingdon, al. 2014; et Kingdon, Lubbe (e.g., freezing may fall below temperatures nighttime savannah monkeys or African green monkeys; population-specific names include population-specific monkeys; green or monkeys African savannah around ~129 kya), after which populations were introduced to several islands in the the in islands several to introduced were which populations after kya), around ~129 from over 1600 free ranging vervet monkeys (the genus Chlorocebus (the vervet monkeys ranging 1600 free from over 1997). Vervets live in multi-male, multi-female groups, with males migrating migrating males with groups, multi-female multi-male, in live Vervets 1997). grivets, malbroucks, and others) from multiple locations spanning the range of the of the range the spanning locations multiple from others) and malbroucks, grivets, become genetically isolated (Svardal et al., 2017). They have been observed living in in living observed They been have 2017). al., (Svardal et isolated genetically become Caribbean from West Africa ~350 years ago (Jasinska et al., 2013; Warren et al., al., et 2013; al., Warren et ago (Jasinska Africayears ~350 from West Caribbean between groups in early adulthood, and groups range in size up to 50 animals, 50 to animals, up size in range groups and early adulthood, groups in between genus. Vervets are highly adaptable, semi-terrestrial foragers, able to occupy a a occupy to able foragers, semi-terrestrial adaptable, highly are Vervets genus. 2015; Svardal et al. 2017). Throughout their evolutionary history in Sub-Saharan Sub-Saharan history in evolutionary their Throughout 2017). al. et 2015; Svardal although most are considerably smaller (Struhsaker, 1967; Hall & Gartlan, 1965; Gartlan, & 1967; Hall (Struhsaker, smaller considerably are although most Africa, these taxa show long histories of gene flow, although they have more recently recently more although have they flow, of gene show long histories taxa these Africa, Fedigan & Fedigan, 1988; Cheney & Seyfarth, 1983; Enstam & Isbell, 2007). Isbell, & Enstam 1983; 1988; Seyfarth, & Cheney Fedigan, & Fedigan Author Manuscript This article isprotected by copyright. All rights reserved. American JournalofPhysicalAnthropology , , and and , cynosuros Ch.
John Wiley&Sons, Inc. Ch. pygerythrus p. ~ 446 kya, and a southern southern a and ~ 446 kya, , which diverged, ~531 kya, ~531 kya, , , called also 6 Page 6of69
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pygerythrus pygerythrus groups within the samples studied in this paper, with with paper, this in studied samples the groups within (2017) use established taxonomic names for genomically clustered population population clustered for genomically names taxonomic established (2017) use distinct populations, with populations, distinct disputed (Warren et al., 2015), as well as the status of these groupings as species species as groupings of these status the well as as 2015), al., et (Warren disputed further discussion of discussion further 2003). Toal. avoid populations sampled from Ethiopia, from Ethiopia, sampled populations Ch. p. pygerythrus p. Ch. Chlorocebus nested in Chlorocebus in nested according to Groves (2001) and Butynski et al. (2013 al. et Butynski and (2001) Groves according to crops and houses for food (Grobler et al. 2006; Brennan et al. 1985; Boulton et al., al., 1985; et al. et Boulton Brennan 2006; al. (Grobler et food for houses and crops (Turner et al., 2016a; Haus et al., 2013) generally supports these taxonomic taxonomic these 2013) supports generally al., et 2016a; Haus al., (Turner et Ch. p. pygerythrus p. Ch. each population by either their country of origin or accepted taxonomic names names taxonomic or accepted country of either by origin their population each populations sampled in St. Kitts & Nevis with an origin in West Africa. Although Africa. West in an with origin Nevis & Kitts in St. sampled populations 1996; Dore, 2013). 2013). 1996; Dore, groupings, although current taxonomic distinctions below the genus level are are level genus the below distinctions taxonomic although current groupings, diagnosable and geographically defined subspecies or species based on phenotypic based phenotypic on or species subspecies defined geographically and diagnosable Svardal et al. recognize recognize al. Svardal et characters (Hill, 1966; Groves, 2001; Grubb et al. 2003). Recent genetic work genetic 2003). al. Recent et 2001; Grubb Groves, 1966; (Hill, characters
Author Manuscript agreed that generally It is h. pygerythrus subsumes taxonomy current , cynosuros Ch. s a into the the into are regarded as pests throughout much of their range since they raid they since range much of their throughout pests as regarded are , or populations sampled from South Africa, and and Africa, from South sampled or populations f and and This article isprotected by copyright. All rights reserved. C or subspecies nested in in nested or subspecies Ch. sabaeus Ch. Ch. p. hilgerti p. Ch. American JournalofPhysicalAnthropology Ch. p. hilgerti p. Ch. John Wiley&Sons, Inc. may be divided into several several divided into may be Chlorocebus .
species or subspecies (Groves 2001; Grubb et (Groves 2001; et Grubb or subspecies species Ch. p. hilgerti p. Ch. and being at least as distinguishable from distinguishable as at least being this taxonomic uncertainty, here we refer to refer we to here uncertainty, taxonomic this Ch. p. p. Ch. pygerythrus Chlorocebus aethiops Chlorocebus or populations sampled in Kenya, Kenya, sampled in or populations f Ch. Ch. hilgerti , p. ): aethiops Ch. describing describing aethiops Ch. Ch. p. hilgerti p. Ch. as two genomically two genomically as Ch. sabaeus Ch. . Svardal et al. al. . Svardal et
Ch. p. p. nd Ch. a Ch. p. p. Ch. f or , , 7
suggested by established hypotheses regarding the evolution of body size: of body evolution size: the regarding hypotheses established suggested by
The breadth of our sample allows us to examine several predictions predictions several examine allows us to sample of our breadth The (3) (2) (1)
body mass. body mass. Rensch’s Rule (Rensch, 1950; Clutton-Brock et al., 1977) hypothesizes that that 1977) hypothesizes al., et 1950; Clutton-Brock (Rensch, Rule Rensch’s sexual dimorphism will be greater in populations that exhibit greater overall greater exhibit that populations in greater be will dimorphism sexual geographically at higher latitudes and altitudes and climatically at lower lower at climatically and altitudes and latitudes higher at geographically temperatures) will have relatively short limbs to preserve body heat. body heat. preserve to short limbs relatively will have temperatures) Allen’s Rule (Allen, 1877) hypothesizes that animals in colder climates (e.g., (e.g., colder climates in animals that hypothesizes 1877) (Allen, Rule Allen’s Bergmann’s Rule (Bergmann, 1847; Meiri & Dayan, 2003) hypothesizes that that 2003) Dayan, hypothesizes 1847; & Meiri (Bergmann, Rule Bergmann’s animals in colder climates (i.e., geographically at higher latitudes and and higher latitudes at geographically (i.e., colder climates in animals altitudes and climatically at lower temperatures) will be larger in body size size body larger in be will lower temperatures) at climatically and altitudes compared to those in warmer climates to stave off the loss of body heat. heat. of loss body off the stave to warmer climates in those to compared a. b. b. Author Manuscripta.
annual and winter temperatures. temperatures. winter and annual warmer experiencing those than limbs shorter will relatively have limbs compared to those in equatorial latitudes and low altitudes. low latitudes altitudes. and equatorial in those to compared limbs short relatively will have altitudes and higher latitudes at Animals Animals experiencing lower mean annual and winter temperatures temperatures winter and annual lower mean experiencing Animals winter temperatures. temperatures. winter and warmer annual experiencing those than body larger size in will be Animals experiencing lower mean annual and winter temperatures temperatures winter and annual lower mean experiencing Animals than those in equatorial latitudes and low altitudes. low and altitudes. latitudes equatorial in those than body size in larger will be altitudes and higher latitudes at Animals This article isprotected by copyright. All rights reserved. American JournalofPhysicalAnthropology John Wiley&Sons, Inc. 8 Page 8of69
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pygerythrus climate. Our largest sample, from South Africa ( Africa from South Our sample, largest climate. Meiri & Dyan, 2003; Dunham et al. 2013; Guillaumet et al. 2008), we have also also 2008), have we al. et 2013; al. 2003; et Guillaumet Dyan, & Dunham Meiri taxonomic categories. We expect this to be particularly noticeable within the larger the within be to particularly noticeable this expect We categories. taxonomic short limbs. Although recent analyses of Bergmann’s and Allen’s Rules show mixed Rules Allen’s and of Bergmann’s analyses recent Although short limbs. Ch. p. hilgerti and p. Ch. intermediate, and local climatic variation ranging from wet and temperate to dry and very cold. dry to cold. very and temperate and wet from ranging variation climatic local and variability. Our sample from St. Kitts and Nevis ( Nevis and Kitts from Our St. sample variability. included these in our analysis. We also predict that patterns of dimorphism within within of dimorphism patterns predict also that We our analysis. in included these
results regarding the importance of any one climatic variable to the patterns noted noted patterns the to variable climatic one of any importance the regarding results low altitudes, high human impacts, and relatively mild and uniformly tropical tropical uniformly and mild relatively and impacts, high human low altitudes, Chlorocebus countries in Sub-Saharan Africa and two islands in the Caribbean (Fig. 1), Caribbean the in two Africa islands and Sub-Saharan in countries in size variation in animals across large geographic areas, including primates (e.g., (e.g., including primates areas, geographic animals in large across variation size in latitude, we predict that (a) predict we latitude, that body size and proportion will follow climatic variability as opposed to to opposed as variability climatic will follow proportion and body size that representing a wide range and mosaic of ecogeographic, anthropogenic, and climatic climatic and anthropogenic, of ecogeographic, mosaic and wide range a representing diverse for all variables, representing high and low altitudes, a range of latitudes, of latitudes, range a low high and altitudes, representing variables, fordiverse all from mid to high altitudes but with a range of human impacts and climatic climatic and impacts of human range a with but high altitudes from mid to variation (Table 1). Our East African sample ( sample African East Our 1). (Table variation
The animals in our sample come from 61 trapping locations across three three across locations from come 61 our trapping sample in animals The Author Manuscript and altitude by variation of geographic analysis traditional Employing nd high-altitude populations in in populations nd high-altitude a will follow the pattern suggested by Rensch’s Rule. We further suggest suggest further We Rule. Rensch’s suggested by pattern the will follow This article isprotected by copyright. All rights reserved. American JournalofPhysicalAnthropology Ch. p. pygerythrus p. Ch. and and John Wiley&Sons, Inc. Ch. aethiops Ch. Ch. hilgerti p. Ch. aethiops ill be the largest, largest, the be ill w Ch. p. pygerythrus p. Ch. the smallest, and (b) (b) and smallest, the Ch. sabaeus Ch. and and should have relatively should relatively have ) come from uniformly from) come uniformly Ch. p. hilgerti p. Ch. Ch. sabaeus Ch. ), is also the most most is the ), also Ch. p. p. Ch. ) comes ) comes
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patterns in variation, we predict that the rate and pattern of growth will also differwill of also growth and rate pattern the we that variation, predict in patterns side of Africa; this should leave them open to higher environmentally mediated mediated higher to environmentally open them leave of should Africa;side this Ch. pygerythrus Ch. across these populations, such that populations that reach a larger adult size will size larger a adult reach that populations such that populations, these across Ch. sabaeus Ch. intrapopulational variance in body size and proportion than what we will see within within will we what see than proportion and body size variance in intrapopulational either be consistently larger throughout development (Smith & Leigh 1998), & and/or (Smith development larger throughout consistently be either South African ( African South show a more exaggerated spurt of growth around pubertal age (Shea 1985). 1985). (Shea age pubertal around of growth spurt exaggerated more show a for all variation in body size. Phenotypic plasticity in body mass is well noted in wild in noted well is body plasticity mass in Phenotypic size. body in for variation all 1997; Turner et al. 2016b). As such, we also predict that: that: predict also we As such, 2016b). al. et 1997; Turner primates, especially in response to environments altered by humans, such as such as humans, by altered environments to response in especially primates,
increased caloric availability due to garbage dumps, human crops and food waste, food and crops waste, human dumps, garbage due to availability caloric increased and laboratory diets (Altmann et al., 1993; Alberts & Altmann 2005; Turner et al. al. et 2005; Turner Altmann & 1993; al., et Alberts (Altmann diets laboratory and (4)
than those found in environments more isolated from human impacts. impacts. human from isolated more environments found in those than environments more highly impacted by humans (e.g., near garbage dumps, near dumps, garbage (e.g., humans by impacted highly more environments crops, or otherwise human-modified areas) will also have larger body mass mass body larger have also will areas) human-modified or otherwise crops, Given previous work showing that developmental variation underlies adult underlies variation developmental that work previous showing Given variability in body mass and length. In particular, populations exposed exposed to populations In particular, length. and body mass in variability Evolutionary responses to local selection pressures, however, cannot account account cannot however, pressures, selection local to responses Evolutionary Author within-population to will lead availability resource human-mediated Local, Manuscript . aethiops or Ch. Ch. p. pygerythrus p. Ch. clade, wherein the distance between Kenyan ( Kenyan between distance the wherein clade, This article isprotected by copyright. All rights reserved. American JournalofPhysicalAnthropology ) populations is over 5000 km along the eastern eastern the along over 5000 km is ) populations John Wiley&Sons, Inc. Ch. p. hilgerti p. Ch. ) and ) and 10 Page 10of69
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parasite and disease variation (Gaetano et al. 2014; Senghore et al., 2016), genital 2016), genital al., et 2014; et Senghore al. (Gaetano variation disease and parasite morphology and appearance (Cramer et al. 2013; Rodriguez et al. 2015a, 2015b), 2015a, al. et 2013; Rodriguez al. (Cramer et appearance and morphology development (Schmitt et al., 2017), genetic/genomic (Jasinska, et al., 2013; al., et Turner (Jasinska, 2017), genetic/genomic al., et (Schmitt development and other biological parameters within the genus genus the within parameters biological other and individual drop traps as described by Brett et al. (1982) and Grobler and Turner (1982) and Grobler al. and et Brett by described as traps drop individual variation (Fourie et al., 2015), C4 isotopes variation in hair (Loudon et al., 2014), gut et (Loudon hair al., in variation C42015), isotopes al., et (Fourie variation et al. 2016a; Warren et al. 2015; Svardal et al., 2017; Schmitt et al., 2017) and al., et 2017; Schmitt al., 2015; et al. et Svardal 2016a; al. Warren et (2010), while trapping in St. Kitts and Nevis was done by local trappers using large using trappers local by done was Nevis and Kitts St. in trapping while (2010), Vervet Research Consortium is a multidisciplinary research group that has, in in has, that group research multidisciplinary a is Consortium Research Vervet
including South Africa, Botswana, Zambia, Ethiopia, The Gambia, Ghana, and on the the on and Ghana, Gambia, The Ethiopia, Zambia, Botswana, Africa, South including protocol: Ethiopia in 1973, Kenya in 1978-79; South Africa in 2002-2008, and and 2002-2008, Africa in 1978-79; South in 1973, Kenya in Ethiopia protocol: transcriptomic (Jasinska et al., 2017) variation, SIV immune response (Ma & & (Ma response 2017) SIV immune variation, al., et (Jasinska transcriptomic group traps (Jasinska et al., 2013). Animals were anesthetized while in the trap and and trap in while the anesthetized were 2013). Animals al., et (Jasinska group traps addition to morphological variation, studied variation in patterns of growth patterns and in variation studied variation, morphological to addition Caribbean islands of St. Kitts and Nevis (Fig. 1). Trapping in Africa employed Africa employed in 1). Trapping (Fig. Nevis and Kitts of St. islands Caribbean several African countries and the Caribbean in 2009-2011 in collaboration with the the with in collaboration 2009-2011 in Caribbean the and countries African several Jasinska et al. 2013; Ma & Jasinska et al. 2014; Svardal et al., 2017), hormonal 2017), hormonal al. al., 2014; et et Svardal Jasinska & al. 2013; et Ma Jasinska then removed to a processing area. Sex was determined by visual and manual manual determined was and visual by Sex area. processing removed a to then International Vervet Research Consortium (Jasinska et al., 2013). The International 2013). International The al., et (Jasinska Consortium Research Vervet International inspection, while age classes were assigned from dental eruption sequences and and sequences eruption dental from assigned were classes age while inspection, Vervet monkeys were trapped at locations across sub-Saharan Africa, Africa, across sub-Saharan locations at trapped were monkeys Vervet Author Manuscript common a using years many over made collections field derive from data The This article isprotected by copyright. All rights reserved. American JournalofPhysicalAnthropology MATERIALS AND METHODS AND METHODS MATERIALS John Wiley&Sons, Inc. Chlorocebus . 11
are known to be descended from West African African West from descended be known to are several hundred years ago (Warren et al. 2015). Of the whole sample, 288 females females 288 Of whole sample, 2015). the al. et (Warren ago years hundred several All animals were released to their social group after sampling and recovery and from sampling after group social their to released were All animals Ethiopia, Ethiopia, based on previous observations (Table 2). All animals were weighed with either an an either with weighed were All 2). animals (Table observations previous on based and 460 males were dentally immature. Sexual maturity is typically not reached in in reached not typically is maturity Sexual immature. dentally were males 460and anesthesia. Observations during trapping allowed us to confirm the animals' social social animals' the confirm to us allowed during Observations trapping anesthesia. electronic or hanging scale, and measured with a tape measure and sliding calipers. calipers. sliding and measure tape a with measured and scale, or hanging electronic here denoted as adult (Bolter & Zihlman, 2003). As is common, dental age and and age dental common, As is 2003). Zihlman, & adult (Bolter as denoted here on the Caribbean islands of St. Kitts and Nevis (Table 3). The Caribbean populations Caribbean The 3). and (Table Nevis Kitts islands of St. Caribbean the on vervets until near the time of canine tooth eruption, here denoting the beginning of the beginning denoting here eruption, tooth of canine time the near until vervets group and local population affiliation. affiliation. population group local and Parameters and protocols describing all measurements are available through available are the measurements all describing protocols and Parameters skeletal age are presumed to be similarly correlated across the genus, meaning that that meaning genus, the across correlated similarly be to presumed are age skeletal length, thigh length, leg length, and foot length) and body mass from a total of 1613 total a from bodyand mass length) foot and leg length, length, thigh length, dental age 6 (Cramer et al., 2013; Rodriguez et al., 2015a); although somatic and and 2015a); somatic although al., 2013; et al., Rodriguez 6 age (Cramer et dental Bones and Behavior Working Group (2015; http://www.bonesandbehavior.org/). http://www.bonesandbehavior.org/). (2015; Group Working Behavior and Bones comparable dental age implies comparable skeletal developmental age across across age developmental skeletal comparable implies age dental comparable vervets in four geographically and genomically distinct populations: populations: distinct genomically and geographically four in vervets skeletal growth often continues beyond the emergence of the third molar, which is which is molar, third of emergence the the beyond continues growthskeletal often populations (Šešelj, 2013). (Šešelj, populations For the present study, we chose metrics representative of skeletal size (body size of skeletal representative metrics chose we study, present the For
Author Manuscript hilgerti p. Ch. This article isprotected by copyright. All rights reserved. in Kenya, in Kenya, American JournalofPhysicalAnthropology Ch. p. p. Ch. pygerythrus John Wiley&Sons, Inc. Ch. sabaeus Ch. n South Africa, and and Africa, South n i brought to the Caribbean Caribbean the brought to in in Ch. aethiops Ch. sabaeus Ch.
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and JDC) were trained directly by TRT. During training, repeated measures of the of the measures repeated training, During TRT. by directly trained were JDC) and same individual were conducted in tandem with TRT until concordance was was concordance TRT with until tandem in conducted were individual same reached. reached. and for most sites measured using hand-held GPS units. For those trapping sites sites trapping those For units. GPS hand-held using measured for sites and most lacking GPS readings, a general latitude and longitude for the trapping area (e.g., (e.g., area for trapping the longitude and latitude general a readings, GPS lacking game reserve, town) was used. Human impact at each trapping location was was location trapping each at impact Human used. was town) reserve, game assessed according to conditions during the time of trapping using a previously previously a using of trapping during time the conditions according to assessed published index developed by Pampush (2010) to study variation in vervet body in study to variation (2010) Pampush by developed index published as native plant productivity) that might also influence body size and growth. As a As a growth. and body size influence also might that productivity) plant native as size, and subsequently used by Loudon et al. (2014) and Fourie et al. (2015) (Table (2015) (Table al. et (2014) Fourie and al. et Loudon used by subsequently and size, proxy for these measures, we collected several climatic variables for trapping sites sites for trapping variables climatic several collected we measures, these proxy for 1). This index includes presence/absence measures of reliable access to 1) to access measures of reliable presence/absence includes index This 1). WorldClim 2 from WorldClim the agricultural land, 2) human food, 3) rubbish or garbage dumps, and 4) whether whether 4) and dumps, garbage or food, 3) rubbish 2) human agricultural land, the ecological impact of humans, and do not address local ecological variables (such variables ecological local address do and not of humans, impact ecological the animals are regularly provisioned, as well as a three-level scale of human activity activity of human scale three-level a well as as regularly are provisioned, animals within the presumed home range of the group (low, moderate, or high). In the index, index, In the or high). moderate, (low, group of the range home presumed the within moderate (index=6-8), to high (index=9-11). These measures take into account only into account take measures These high (index=9-11). to (index=6-8), moderate point values are assigned to each value, with the lowest tier of human impact each each impact of human tier lowest the with value, assigned each are to values point receiving a 1, scaling up by 1 for each level. Added together, these values comprise a a comprise values these together, Added 1 by level. for up each scaling 1, a receiving human impact group ranging from low (lowest score in each category; index=5), to to category; index=5), each in score (lowest from low group ranging impact human All measurements were developed by CJJ and TRT and other measurers (CAS (CAS measurers other and TRT and CJJ by developed were All measurements Author Manuscript 1), in (Table degrees reported decimal site is trapping of each location The This article isprotected by copyright. All rights reserved. database, which has a spatial resolution of about 1 km of about resolution spatial a which has database, American JournalofPhysicalAnthropology John Wiley&Sons, Inc. 2 (Fick (Fick 13
sizes and differences in variance structure across age/sex/taxon categories, we we categories, age/sex/taxon across structure variance in differences and sizes variables on adult body mass and length. We used the absolute value of latitude to to latitude of value absolute used the We length. and mass adult body on variables (Hijmans & van Etten, 2012), and assigned to trapping sites based on latitude and on based sites trapping to 2012), assigned van and & Etten, (Hijmans (Peters, 2015) in R v. 3.2.0 (R Core Team 2017). We used linear mixed modeling, mixed modeling, Weused linear 2017). (R Core Team 2015) 3.2.0 Rv. in (Peters, assessed differences in mean measures using a Welch ANOVA with a Games-Howell Games-Howell a with Welch ANOVA a using measures mean in differences assessed monthly precipitation). Climate data were accessed via the R package Rpackage the via accessed were data Climate precipitation). monthly allow for negative latitudinal values in the southern hemisphere. We included We hemisphere. southern the in values latitudinal allow for negative longitude. longitude. also implemented in R, to assess the influence of latitude (in decimal degrees), degrees), decimal (in of influence latitude the R, assess to in implemented also post hoc Tukey post & Hijmans, 2017). Climatic variables considered for inclusion in our models were 1) were models our in for considered inclusion variables 2017). Climatic Hijmans, & deviation for each population and age category (Table 3) Due to the uneven sample sample uneven the 3) to Due (Table category age and population for each deviation country of origin as a random effect to control for potentially uncontrolled effects effects uncontrolled potentially for control to random effect a as country of origin altitude (in meters), human impacts (using the human impact group), and climatic climatic and group), impact human the (using impacts human meters), (in altitude annual mean temperature (in degrees Celsius), 2) temperature seasonality seasonality 2) temperature Celsius), degrees (in temperature mean annual that might be the result of large-scale population differences. With models fit in in fit models With differences. population of result large-scale the be might that mm), and 6) precipitation seasonality (measured as the coefficient of variation of of variation coefficient the as (measured seasonality 6) and precipitation mm), (measured as the standard deviation of annual mean temperature multiplied by by multiplied temperature mean of annual deviation standard the as (measured 100), 3) the minimum temperature of the coldest month (in degrees Celsius), 4) the 4) the Celsius), degrees (in month coldest of the temperature 100), minimum 3) the mean temperature of the coldest quarter of the year, 5) annual precipitation (in (in precipitation 5) annual year, of the quarter coldest of the temperature mean
Author Manuscript ± standard mean as presented are measures of somatic statistics Summary analyses Statistical test implemented using the package the using implemented test This article isprotected by copyright. All rights reserved. American JournalofPhysicalAnthropology John Wiley&Sons, Inc. userfriendlyscience raster v. 03-0 v. v. 2.6-7 v. 14 Page 14of69
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using the R the using dimorphism for each taxon was measured as the average mass of adult males males of adult mass average the as measured was taxon fordimorphism each correction for finite sample sizes (AICc) to compare models with differing fixed differing models with (AICc) sizes compare to sample for finite correction 2.1-1 (Mazerolle, 2017). Final models were assessed for goodness of fit to the data data the to of fit for goodness assessed models were Final 2017). 2.1-1 (Mazerolle, divided by the average mass of adult females (Smith 1999). We assessed whether whether 1999). assessed We (Smith of adult females mass average divided the by effects structures (Burnham & Anderson, 2002) using the package package using the 2002) Anderson, & (Burnham structures effects (2013), implemented in the package package in the implemented (2013), lme4 for sexual dimorphism, all models were run separately for males and females. Sexual Sexual females. and for males run separately models were all dimorphism, for sexual distribution. distribution. effects only in the package package the only in effects MCMC-estimated P MCMC-estimated to body length, respectively (e.g., thigh length/body length). We used the methods methods used the We length). length/body thigh (e.g., respectively bodyto length, above to fit generalized linear mixed models for the hind limb proportions with the the with proportions limb hind the mixed models for linear generalized fit to above ran 100,000 iterations and sampled every 20 sampled and 100,000 iterations ran 0.8.3.3 (Fournier et al., 2012) to appropriately model proportions, with country with of model proportions, appropriately 2012) to al., et (Fournier 0.8.3.3 exception that models were fit with a beta distribution in the package package the in distribution beta a with fit models were that exception origin as a random effect. We selected the best model based on comparatively comparatively on model best based the selected We random effect. a as origin final models in the package package the models in final lowest AIC using the package package the using AIClowest We allowed the Markov chains a burn-in period of 1,000 iterations, after which we we which after of 1,000 period iterations, burn-in a chains Markov allowed the We of-fit, pseudo- of-fit, v. 1.1-13 (Bates et al., 2015), we used the Akaike Information Criterion with a a with Criterion Information Akaike 2015), used we the al., et 1.1-13 v. (Bates Author Manuscript segment limb of each ratio the as measured were lengths limb hind Relative 2 for mixed models method reported by Nakagawa and Schielzeth Schielzeth and Nakagawa by reported models method for mixed R 2 values for the best beta regression models were derived from fixed from derived models were regression beta for best the values values to assess the significance of ( fixed effects significance the assess to values This article isprotected by copyright. All rights reserved. American JournalofPhysicalAnthropology v. 3.1-0 (Cribari-Neto & Zeileis, 2010). To allow Zeileis, & 3.1-0 v. (Cribari-Neto betareg MCMCglmm bbmle John Wiley&Sons, Inc. v. 1.0.20 (Bolker, 2017). (Bolker, 1.0.20 v. MuMIn v. 2.24 (Hadfield, 2010), using flat priors. priors. flat using 2010), (Hadfield, 2.24 v. v. 1.15.6 (Barton, 2016). We used We 2016). (Barton, 1.15.6 v. th iteration for posterior the iteration To estimate goodness- To estimate AICcmodavg α = 0.05) for = the 0.05) glmmADMB v. v. v. v. 15
typically not between sexes (Smith et al., 1994). Turner et al. (1997) and Bolter and and (1997) Bolter and al. et Turner 1994). al., et sexes (Smith between not typically Zihlman (2003) have suggested that, in vervets ( vervets in that, (2003) suggested have Zihlman age at particular tooth eruption can vary both within and across taxa, although taxa, across and vary within can both eruption tooth particular at age differences in sexual dimorphism between populations were significant using the the using significant were populations between dimorphism sexual in differences method of Relethford and Hodges (1985). (1985). Hodges and ofmethod Relethford of chronological ages may be encompassed within a single dental age category, as as category, age dental single a within encompassed be may ages of chronological respectively), these dental age categories represent uneven, approximately 3-12 uneven, represent dental categories age these respectively), chronological age range encompassed by of ‘adult’ age assignment, here after the the after here assignment, age of by ‘adult’ encompassed range chronological age measurement data on wild individuals of known ages will be necessary to validate validate to necessary will be ages of known wild on individuals data measurement month periods of age up until adulthood, which contains all adults from the eruption eruption the from adults all contains which adulthood, until up of age periods month chronological age categories from within the range suggested by previous work work previous suggested by range the from within categories chronological age emergence of the third molar, obscures the pattern of any further growth. growth. furtherof any pattern the obscures molar, third of the emergence this assumption. This interpretation of growth is limited, however, to those intervals intervals those to however, of growth limited, is interpretation This assumption. this of the third molar onward (Table 2). Here, we interpret significant changes in size size changes in significant interpret we Here, 2). (Table onward third molar of the samples (e.g., Leigh 1992; Leigh & Shea 1996). We modeled each trait in each sex sex each in modeled trait We each 1996). 1992; Shea Leigh & (e.g., Leigh samples represented by age categories 6 and prior, after which point the relatively wide relatively the which point after categories 6 prior, age by and represented loess smoothers, or nonparametric locally weighted quadratic least squares squares least quadratic locally weighted or nonparametric smoothers, loess between these categories as indicative of patterns of growth. Longitudinal Longitudinal of growth. of patterns indicative categories as these between within each taxon separately. We attempted this model fitting using estimated estimated using fitting model this attempted We separately. taxon each within regression, implemented in in implemented regression, make no assumptions about the shape of the curve, and are robust to uneven uneven to robust are and curve, of the shape about the assumptions no make In our data set, relying on cross-sectional dental eruption means that that range a means eruption dental cross-sectional on relying In our set, data Author using taxa across and within growth patterns compare and visualize We Manuscript This article isprotected by copyright. All rights reserved. American JournalofPhysicalAnthropology ggplot2 John Wiley&Sons, Inc. (Wickham, 2009). Localized loess smoothers smoothers loess (Wickham, Localized 2009). Ch. p. hilgerti p. Ch. and and , Ch. , tantalus 16 Page 16of69
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pygerythrus pygerythrus with body mass increasing as latitude increases ( increases latitude as increasing bodywith mass significant positive relationship between body mass and latitude in adult females, adult females, in latitude and body mass between relationship positive significant designation and geographic origin were modeled as random effects. For all tests, we we tests, all For random effects. as modeled were origin geographic and designation Prediction 1: Population variation in vervet body size will follow Bergmann’s Rule Rule Bergmann’s follow vervet body will in size variation Population 1: Prediction considered a a considered
(larger in higher latitudes and altitudes). altitudes). and latitudes in higher (larger chronological age categories were treated as continuous variables, and and taxonomic variables, continuous as treated were categories chronological age they experience a steep increase in mass that nearly catches up in size to to size in up nearly that catches mass in steep a increase experience they (Turner et al., 1997; Bolter & Zihlman, 2003). In loess models, estimated estimated models, loess 2003). In Zihlman, & 1997; Bolter al., (Turner et 2a; Table 3), significantly so for dental ages 1 (p < 0.05), 6 (p < 0.001; all populations populations all 0.001; < < 6 1 0.05), (p (p ages dental for so significantly 3), 2a; Table latitude latitude 34 populations for most of development, between dental between for of development, most populations aethiops Ch. and The Gambia) maintain an intermediate mass similar to the sampled sampled similar the to mass an intermediate maintain Gambia) The but but sooner in adulthood than in adulthood than in sooner 0.690; Table 4), but not with altitude ( altitude with not but 4), Table 0.690; female body mass suggest that the high latitude high latitude the that suggest body mass female ° S) maintains a heavier mass than all other taxa throughout development (Fig. (Fig. development throughout taxa other all than mass heavier a maintains S) Ch. sabaeus Ch. As predicted and consistent with Bergmann’s Rule, our linear model shows a a model shows our linear Rule, Bergmann’s with consistent and As predicted Author sabaeus Ch. Manuscript females. This sabaeus growth Ch. rapid in females. P value of less than 0.05 to be significant. significant. 0.05 be to than less of value ), and adults (p < 0.001). Although females of the i of the females Although < 0.001). (p adults and ), (17 population This article isprotected by copyright. All rights reserved. American JournalofPhysicalAnthropology Ch. p. pygerythrus p. Ch. John Wiley&Sons, Inc. °
N in St. Kitts; 13 St. in N RESULTS β = 0.000, p = 0.678). Loess curves for adult curves = 0.678). Loess p = 0.000, , as,
Ch. p. pygerythrus p. Ch. β the latter the = 0.033, p = R = 0.022; p 0.033, ° females apparently off levels females N in ancestral populations in in populations ancestral in N females ultimately reach reach ultimately females ntermediate ntermediate (23 population Ch. p. hilgerti p. Ch. 5 6 and ages 2 GLMM(c) Ch. p. p. Ch. =
°
17 – –
for much of their development. development. for much of their sabaeus Chlorocebus exception that female female that exception Ch. p. pygerythrus larger p. Ch. the between relationship Although 4). size the Table Chlorocebus Ch. p. pygerythrus p. of Ch. mass the match eventually to onward Age 2 from Dental a significantly higher average adult size. The lower latitude, East African African East latitude, lower The adult size. higher average significantly a maintain masses similar to each other throughout the life course, with the notable notable the with course, life the similar throughout other masses each to maintain females being the smallest, mid-range mid-range smallest, the being females males is unexpected within the context of Bergmann’s Rule (Fig. 2b; Table 4). 4). 2b; Table (Fig. Rule of Bergmann’s context the within unexpected is males Table 4) Table variation seen in males, as there is no significant relationship between between and body size relationship significant no is males, there in as seen variation 1, but grow rapidly at this stage to catch up to to up catch to stage this at grow but 1, rapidly Bergmann’s Rule is supported, with significant positive relationships between body between relationships positive significant with supported, is Rule Bergmann’s Ch. p. pygerythrus p. Ch. both than smaller significantly and size, in matched Ch. sabaeus Ch. the when Indeed, the high latitude high latitude the latitude ( latitude by dental age 2. The end result of these growth patterns is a scale of mass scale in a is patterns growth of result these end The 2. age dental by weight and both latitude ( latitude both and weight Ch. sabaeus growth of Ch. rapid relatively the holds, taxa African East smaller The scaling of Bergmann’s Rule, however, does not adequately describe the the describe adequately not does however, Rule, of Bergmann’s scaling The . Both Both β
Author Manuscript ( = = altitude 0.231) -0.358, p or females females that follows Bergmann’s Rule, with the equatorial East African African East equatorial the with Rule, that follows females Bergmann’s Ch. p. hilgerti p. Ch. Ch. p. pygerythrus p. Ch. , This article isprotected by copyright. All rights reserved. Ch. p. hilgerti p. Ch. are much smaller than all other taxa at dental age age dental at taxa other all than much smaller are Ch. aethiops American JournalofPhysicalAnthropology β = 0.083, p = 0.006) and altitude ( altitude and = = 0.006) p 0.083, and and males are removed from the regression equation, equation, removed are from regression the males males, like the females, remain females, the like males, aethiops Ch. John Wiley&Sons, Inc. (3 S – 1 – S females being the largest. largest. being the females °
Ch. sabaeus Ch. β ° (7 aethiops Ch. N) and = -0.011, = R 0.179; p Ch. p. hilgerti p. Ch. emales being intermediate, and and intermediate, being emales f and β = 0.001, p = = 0.011; p 0.001, – 12 – Ch. sabaeus Ch. 2 ° GLMM(c)
and ° N), N), = 0.616; males males Ch. Ch. females females adult a nd 18 Page 18of69
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consistent with Bergmann’s Rule, slightly larger negative effects on body mass of the of body the mass on effects negative slightly larger Rule, Bergmann’s with consistent seasonal rainfall, which may also be consistent with Bergmann’s Rule. For the sake sake the For Rule. Bergmann’s with consistent be which may also rainfall, seasonal minimum temperature of the coldest month ( month coldest of the temperature minimum of consistency, we also ran the global model with climatic variables on males males on variables climatic model global with the ran also we of consistency, for the adult equatorial for adult equatorial the mass of any covariate considered (Table 5). In males, there were significant but but significant were there males, In 5). (Table considered covariate of any mass negative relationship between body mass and precipitation seasonality ( precipitation and body mass between relationship negative excluding negligibly small effects of temperature seasonality and annual precipitation, and, and, precipitation, annual and seasonality of temperature effects small negligibly p < 0.001; Table 5) suggests that male body size may decrease in areas with highly with areas in decrease may body size male that 5) suggests