Ecogeographical Variation in Skull Shape of South-American Canids: Abiotic or Biotic Processes?

15 Pages·2015·2.2 MB·English

by  Jamile Moura Bubadué

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Bubadue, J, Caceres, N, Carvalho, R and Meloro, C
Ecogeographical Variation in Skull Shape of South-American Canids: Abiotic
or Biotic Processes?
http://researchonline.ljmu.ac.uk/id/eprint/2846/
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Bubadue, J, Caceres, N, Carvalho, R and Meloro, C (2015) Ecogeographical
Variation in Skull Shape of South-American Canids: Abiotic or Biotic
Processes? Evolutionary Biology. pp. 1-15. ISSN 1934-2845
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EvolBiol
DOI10.1007/s11692-015-9362-3
RESEARCH ARTICLE
Ecogeographical Variation in Skull Shape of South-American
Canids: Abiotic or Biotic Processes?
Jamile de Moura Bubadue´1 • Nilton Ca´ceres2 • Renan dos Santos Carvalho2 •
Carlo Meloro3
Received:2July2015/Accepted:31October2015
(cid:2)TheAuthor(s)2015.ThisarticleispublishedwithopenaccessatSpringerlink.com
Abstract Species morphological changes can be mutu- skull size and shape. The hypercarnivorous bush dog is
ally influenced by environmental or biotic factors, such as mostly distinct in shape from all the other taxa while a
competition. South American canids represent a quite degree of overlap in shape—but not size—occurs between
recentradiationoftaxathatevolvedformsverydisparatein species of the genus Lycalopex. Both climate and compe-
phenotype, ecology and behaviour. Today, in the central tition impacts interspecific morphological variation. We
part of South America there is one dominant large species identifiedclimaticadaptations asthemain driving force of
(the maned wolf, Chrysocyon brachyurus) that directly diversificationfortheSouthAmericancanids.Competition
influence sympatric smaller taxa via interspecific killing. has a lower degree of impact on their skull morphology
Further south, three species of similar sized foxes (Lyca- althoughitmighthaveplayedaroleinthepast,whencanid
lopex spp.) share the same habitats. Such unique combi- community was richer in morphotypes.
nation of taxa and geographic distribution makes South
American dogs an ideal group to test for the simultaneous Keywords Canidae (cid:2) Carnivora (cid:2) Climatic adaptations (cid:2)
impactofclimateandcompetitiononphenotypicvariation. Geographic clines (cid:2) Interspecific competition (cid:2)
Using geometric morphometrics, we quantified skull size Macroecology
and shape of 431 specimens belonging to the eight extant
South American canid species: Atelocynus microtis, Cer-
docyon thous, Ch. brachyurus, Lycalopex culpaeus, L. Introduction
griseus,L.gymnocercus,L.vetulusandSpeothosvenaticus.
South American canids are significantly different in both Understanding species community assembly is one of the
central aims of macroecology (Rosenzweig 1995). For
instance,ontheoneside,weexpectabioticforces,suchas
Electronicsupplementarymaterial Theonlineversionofthis
climate and geographical barriers, to apply filters influ-
article(doi:10.1007/s11692-015-9362-3)containssupplementary
material,whichisavailabletoauthorizedusers. encing species distribution and community composition.
On the other side, biotic competition might produce
& CarloMeloro
unexpectedly stable species assemblages. Such balancing
[email protected]
forces are clearly not mutually exclusive and we have
1 ProgramadePo´s-Graduac¸a˜oemBiodiversidadeAnimal, strong evidence that the majority of animal groups tend to
CCNE,FederalUniversityofSantaMaria,SantaMaria, be quite resilient and less sensitive to abiotic forces than
RS97110-970,Brazil
expected by theory (Vrba 1993). In this regards, members
2 DepartmentofEcologyandEvolution,CCNE,Federal of the mammalian order Carnivora received particular
UniversityofSantaMaria,SantaMaria,RS97110-970,
attention for being endothermic, ecologically diverse and
Brazil
secondary consumers (Goswami 2010). The red fox
3 ResearchCentreinEvolutionaryAnthropologyand
(Vulpes vulpes), for instance, is the commonest species to
Palaeoecology,SchoolofNaturalSciencesandPsychology,
provide evidence for the impact of climate on phenotypes,
LiverpoolJohnMooresUniversity,ByromStreet,
LiverpoolL33AF,UK particularly in skull size, which varies with latitude
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EvolBiol
(Churcher 1960; Davis 1977; Cavallini 1995; Yom-Tov butlittleisknownabouttheimpactofcompetitionontheir
and Geffen 2006; Meiri et al. 2007; Yom-Tov et al. 2007; intra and interspecific variation. Wayne et al. (1989)
Szuma2008).Otherlinesofinvestigationsoncarnivorans’ identified high degree of morphological divergence
skull took direct competition into account for explaining between South-American foxes in spite of their relatively
carnivoranassemblyrules(Dayanetal.1989,1992;Dayan short time of divergence (\250,000 years) and we might
and Simberloff 2005; Meiri et al. 2011). expect this to occur even strongly when larger taxa are
Carnivora generally exhibit broad range of ecological included.
and phenotypic variation accompanied by behavioural By focusing our investigation on both climate and
attributes (e.g. predatory/killing behaviour) that makes competition, we aim to provide a fully comprehensive
them particularly sensible to biotic processes (Palomares framework to interpret skull morphology of the extant
and Caro 1999; Donadio and Buskirk 2006). Here, we use South-American canids at broad, continental scale. We
South-American canids as model species to test the opted to quantify skull size and shape by using geometric
hypothesisthatclimateandcompetitionmighthaveadirect morphometricsasagoodproxyforphenotypicvariationat
impact on species morphological variation at broad geo- broad geographical scale (see also Ca´ceres et al. 2014;
graphical scale. South-American canids represent a recent Meloro et al. 2014a, b). This method was favoured among
radiation due to their late Pliocene colonization from a others because it allows direct and independent visualiza-
restricted pool of North American taxa (Berta 1987; Pre- tions of size and shape patterns together with higher sta-
vosti 2010; Perini et al. 2010; Wang et al. 2008). Despite tistical power with reasonably large sample sizes (Adams
this, South America holds more than 10 living canid spe- et al. 2004, 2013).
cies,beingthelargestextantregionaldiversityfoundinthe More specifically our aim is to test the following
world (Prevosti et al. 2009a; Perini et al. 2010; Sillero- hypotheses:
Zubirietal.2004).Itsendemictaxaincludesspecieswitha
1. South American canids differ in both skull size and
broad diversity of body size and feeding ecology such as
shape;
thelarge (average mass = 25 kg)omnivorousmanedwolf
2. Size influences shape differences between species;
Chrysocyonbrachyurus(Illiger,1815)andthesmall(mass
3. Skull shape and size co-vary with climatic variables
ranging 5–8 kg) hypercarnivorous bush dog Speothos
and degree of competition across species;
venaticus (Lund, 1842) (Sillero-Zubiri et al. 2004).
4. Species follow distinct phenotypic patterns of skull
Diversity of fox-like ecomorphs is also broad including
shape changes in relation to broad environmental
species such as the widely distributed crab-eating fox
variables or to different degrees of competition.
(Cerdocyon thous) and the four species of Lycalopex that
share to some extent geographic range, especially in Hypothesis 1 concerns the biological paradigm of
Argentina, and omnivorous feeding habits. Such a high interspecific differentiation and functional convergence.
diversity was even higher during the prehistory (Prevosti Functional convergence in the skull of carnivorans has
2010; Perini et al. 2010) with larger carnivorous wolflike been very often detected in relation to extreme feeding
forms possibly influencing ecology and distribution of adaptations(e.g.durophagy,Figueiridoetal.2011,2013or
smaller taxa. solitary hunting, Meloro et al. 2015a). Meloro (2011),
Currently, we have direct evidence on the impact of MeloroandRaia(2010)andMeloroandO’Higgins(2011)
competition on ecology and behaviour of extant South- identified morphological similarities also between omni-
American canids. Di Bitetti et al. (2009) recorded patterns vores(i.e.,canidsandviverrids)andwemightexpectsome
of behavioural shift by Lycalopex gymnocercus due to overlap between South-American taxa with similar diet.
competition with C. thous. In sympatry, L. gymnocercus Hypothesis2relatestotherecentfindingsbyCa´ceresetal.
changes its normal activity to prevent confrontation with (2014) and Meloro et al. (2014a, b) on geographical vari-
the larger C. thous. Also, interspecific killing occurs quite ation of capuchin and howler monkeys: in these cases a
intensively, with large taxa, such as Ch. brachyurus, gen- significant allometric component was detected also across
erally controlling densities and behaviour of smaller spe- geographic localities so that skull shape differences were
cies (Donadio and Buskirk 2006; Oliveira and Pereira mostly influenced by size.
2014). Hypotheses 3 and 4 relate to ecogeographical pattern
Skulls of South-American wild dogs received reason- generally identifiable in the mammalian skull (Cardini
able attention to clarify patterns of growth and taxonomy et al. 2007). If abiotic forces are more relevant to regulate
(Segura and Prevosti 2012; Segura 2013), paleobiological canid community assembly we might expect stronger co-
and ecological adaptations (Prevosti et al. 2005; Prevosti variation between skull morphology and climate then
et al. 2009a, b), and more recently climatic impact between skull morphology and competition. The opposite
(Machado and Hingst-Zaher 2009; Martinez et al. 2013), might occur if biotic forces are more relevant.
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EvolBiol
Materials and Methods images and minimizes deformation due to the lenses (as
in Meloro et al. 2008). When taking pictures, we set up
Raw Data and Geometric Morphometrics a scale bar adjacent to the specimen in order to trans-
form digital pixels in linear measurements (Zelditch
Our sample includes skull pictures in ventral view of 431 et al. 2004).
wild-caught adult canid specimens of South America Ventral view was chosen because the palate of canids
(Online Resource). For each specimen we recorded the is relatively flat and the teeth can be individually recog-
geographiccoordinatesofitscollectionlocalityresultingin nized. Digital photographs were landmarked by one of us
262 different localities covering seven countries (Fig. 1; (JMB) using the tpsDig2 ver. 2.16 (Rohlf 2015). Land-
see also Table 1). marking by only one investigator allowed to minimize
Skull pictures were taken at fixed distance (2 m). inter-observer error and repeated sessions on 10 random
This procedure standardizes the sample of digital specimens were taken to assess landmark repeatability
Fig.1 MapofSouthAmerica
showingthegeographic
distributionofcanidskull
specimens.Samplinglocalities
ofdifferentspeciesareshown
bydifferentsymbols
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EvolBiol
Table1 Skullsamplesizefor
Species #Specimens #Females #Males Undet
theeightspeciesofcanids
includedinthisstudy
Atelocynusmicrotis(Sclater,1882) 4 1 3 0
Cerdocyonthous(Linnaeus,1766) 227 71 94 62
Chrysocyonbrachyurus(Illiger,1815) 25 5 7 13
Lycalopexculpaeus(Molina,1782) 13 5 4 4
Lycalopexgriseus(Gray,1837) 32 9 4 19
Lycalopexgymnocercus(Fischer,1814) 99 38 28 33
Lycalopexvetulus(Lund,1842) 16 7 5 4
Speothosvenaticus(Lund,1842) 15 3 10 2
Total 431 139 155 137
Fig.2 Disposition of 29 landmarks on a skull of Chrysocyon length; 12–14 fourth pre-molar (carnassial) area; 15–17 first molar
brachyurus specimen. 1 Midpoint of central incisors; 2 posterior- area;18mostposteriortipofthepalatine;19–22zygomaticarcharea;
mostpointoflateralincisoralveolus;3–5caninearea;6–7firstpre- 23tipofparacondylarprocess;24–26occipitalcondylearea;27–29
molar length; 8–9 second pre-molar length; 10–11 third pre-molar auditorybullaarea
(Cardini and Tongiorgi 2003; Meloro 2011; Meloro et al. Statistical Analyses
2014a).
In order to describe effectively craniodental morphol- Taxonomy and Sexual Dimorphism
ogy, we digitized 29 homologous landmarks (Fig. 2). The
landmarks recorded the overall skull shape, zygomatic Topreventpseudoreplicationandhavebetterestimationof
arch, rostrum (palate), auditory bulla, and position and shapeandsizeineachlocality,weusedtheaveragevalues
size of the teeth, being all features generally related to ofourgeometricmorphometricresultsperlocalityandsex
feeding adaptations in Carnivora and Canidae (Schutz inallstatisticalanalyses(Cardinietal.2007;Ca´ceresetal.
et al. 2009; Segura and Prevosti 2012; Meloro et al. 2014).
2015b). We used ANOVA and MANOVA to test if canid spe-
Generalized procrustes analysis (GPA, Rohlf and Slice cies,usedasfactornamed‘‘taxonomy’’,differinskullsize
1990) allowed us to remove from the original landmark and shape. Sex was also included as factor in the models
coordinates differences in size, position and orientation. where taxonomy and sex were tested for interaction (Car-
This procedure transforms raw landmarks coordinates into dini and Elton 2008). Scores of a selection of Relative
shape variables: the procrustes coordinates. The GPA Warp axes that explained at least 95 % of variance were
coordinates were projected into a weight matrix to char- included as dependent variables in the MANOVA models
acterize shape using non-affine (Partial Warps) and affine to reduce degrees of freedom in relation to sample size of
(uniform) components of thin plate spline. A principal particularly small groups (Meloro and O’Higgins 2011).
component analysis of the weight matrix (=relative warp
analysis, RWA) allowed us to visualize shape changes of Allometry
each specimen relative to the mean shape (Zelditch et al.
2004). Skull size was directly extrapolated from raw In order to quantify the allometric effects on our sample,
landmarkcoordinatesusingthecentroidsize(Rohlf2000). we used the natural log transformed centroid size (=lnCS)
WeusedthesoftwaretpsRelwversion1.49(Rohlf2015)to inalltheanalysesasanindependentvariable.Thestrength
computeGPA,extracttheweightmatrix,andtocomputea of allometric signal was tested separately in the whole
RWA. (N = 461) and in the locality averaged sample (N = 262)
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EvolBiol
ofskullsusingMorphoJ(Klingenberg2011)byperforming throughDonadioandBuskirk(2006)arcsinesquarerootof
a multivariate regression of lnCS on skull shape (cf. BSC defined as the body size difference for each species
Ca´ceresetal.2014;Meloroetal.2014a,b).Togetherwith pair, which is calculated through the equation BSD =
global allometry (that assumes no difference in slope (Mb - Mb)/Mb, where Mb is the mass of the larger
l s l l
occurs between species subgroups) we also tested for speciesandMb themassofthesmallerone.Iftheresultof
p s
allometry using pooled regression within subgroups arcsine ffiBffiffiSffiffiffiDffiffiffi was between 2 and 5.4, than we could
(Klingenberg 1996). Using the R environment, version consider the pair of species as potential competitors
2.8.1 (R Development Core Team 2013) and the package directlyinfluencingeachotherviainterspecifickilling(see
geomorph(AdamsandOtarola-Castillo2013)wetestedfor DonadioandBuskirk2006formoredetails).Forexample,
differencesinallometricslopebetweenspecies byrunning atlocalityXwerecordedaskullofC.thous.Inthislocality
an ANOVA model with interaction using shape (as pro- the species could potentially interact with L. gymnocercus
crustesdistances)asdependentvariable,lnCSascovariate duetohabitatpreference(opengrasslands)anddietoverlap
andspeciesasfactor.Werun9999permutationstovalidate (Vieira and Port 2007), but not by interspecific killing
reliability of the P value. Additionally, the global and because the pair C. thous and L. gymnocercus has arcsine
p
locality averaged skull sample were subdivided into single ffiffiffiffiffiffiffiffiffi
BSD lower than two (see Donadio and Buskirk 2006).
speciesdatasetinordertoidentifythestrengthofallometry
Speothosvenaticusisalsopresentatthislocality.Thislast
in different taxa and link these results to taxon-specific
speciesisnotapotentialcompetitorwithC.thousinanyof
p
variation partitioning models (see below). ffiffiffiffiffiffiffiffiffi
our factors because this pair of species arcsine BSD is
lowerthan2(seeDonadioandBuskirk2006).Theydonot
Ecogeographical Variation
overlap in dietary adaptation due to the fact that C. thous
presents an omnivorous diet while S. venaticus is a spe-
To test for the impact of geography on skull shape we
cializedmeateater.Forhabitatpreference,C.thousprefers
employedeachspecimen collectionlocalitytoextract nine-
open grassland areas (Berta 1982) and S. venaticus is pri-
teen bioclimatic variables with a resolution of 100 from the
marily a forest dweller (Oliveira 2009). Thus, we have a
WorldClimrasterdatabase(Hijmansetal.2005)byusingthe
value of 0 for interspecific killing and 0.5 for diet and 0.5
DIVA-GIS7.5software(http://www.diva-gis.org/download).
forhabitat(halfofthespeciesinthatlocationisapotential
Two block partial least squares (=PLS; Rohlf and Corti
competitor due to diet and habitat preferences). We per-
2000)wasappliedusingtpsPLSv.1.18(Rohlf2015)totest
formed this calculation for every specimen, constructing a
the relationship between climate and skull shape. PLS
table that was then used to test competition via PLS
extracts vectors from the correlation matrix of each block
between shape or size and the competition data matrix.
so that the degree of co-variation between one block and
theotherismaximized(RohlfandCorti2000).InMorphoJ
Angular Comparison
(Klingenberg 2011) we also employed PLS to test the
correlation between size (lnCS) and the 19 bioclimatic
After assessing via PLS the impact of climate and compe-
variables. Although this procedure generates only one pair
tition versusskullshape,MorphoJ1.05(Klingenberg 2011)
of vectors, it allows performing comparisons with PLS
was used to compare the direction of PLS shape vectors
vectors obtained for shape (see Meloro and Jones 2012).
extracted for climate and competition, separately. This
providesadirecttesttoassesstheimpactofthesefactorson
Competition
shapingcanidcommunitiesandphenotypicchanges.Sucha
test was not available for PLS size for which we opted to
To identify the possible impact of competition on skull
simplycomparestrengthofcorrelationbetweenthesamples.
shape and size we ascribed to each geographic locality the
If climate impacts size more strongly than competition we
presence/absence of distinct canid species that were char-
might expect higher correlation coefficient (=r) in PLS.
acterized according to their diet, body mass, and biome
preference (Sillero-Zubiri et al. 2004).
For each focal species recorded at a certain locality we Variation Partitioning
recorded the number of canid taxa that could potentially
interactwithitduetodietaryadaptation,habitatpreference We employed variation partitioning (Diniz-Filho and Bini
andbodysize.Foreachlocalitywerecordedthenumberof 2008;Raiaetal.2010;Meloroetal.2014a)toevaluatethe
canids with the same diet and habitat and standardized singular contribution to skull shape variance of four dis-
these values for the total number of species potentially tinct components: taxonomy (described by the categorical
present. Index for assessing the potential of interspecific variable ‘‘species’’), size (described by lnCS), climate (de-
killing (here named body size factor) was computed scribedbythenineteenbioclimaticindices)andcompetition
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EvolBiol
(described by the three variables of size, diet and biome variance) versus the second (19.96 %) RWs evidence
overlap between the species). These factors are all consid- extensive overlap between the different canids’ species,
eredaspredictors(X)ofskullshape(Y,describedbythe54 althoughRW1separatesgenera,showingsomesegregation
shape variables, 2n - 4 where n is the number of land- between almost all Lycalopex spp. and the others (Fig. 3).
marks, Rohlf and Slice 1990) into multiple multivariate OnlyS.venaticusdidnotoverlapwithothersspecies.RW1
regression models. We tested for the effect of each single describeschangesinthezygomaticarch,occipitalcondyle,
factor in isolation and in interaction with each other using auditory bulla, muzzle and teeth. Species at the extreme
the R package vegan 2.0 (Oksanen et al. 2012). We also negative of RW1 exhibit smaller zygomatic arch, occipital
analyzed the contribution of different predictors into size condyle and auditory bulla, more elongated and thinner
variation. We performed variation partitioning between all muzzle,largerfirstmolarandcarnassialandsmallercanine
the average per localities (N = 262; using taxonomy, cli- and incisors. The RW2 describes shape changes related to
mate and competition as factors). These procedures were braincase, zygomatic arch, occipital condyle, auditory
employed for the overall sample of South-American canids bulla, muzzle area and teeth row positioning and size. On
and nested subsets of the genera Cerdocyon and Lycalopex the negative scores of RW2 specimens have larger brain-
that got sufficient data to be considered separately. Since case,zygomaticarch,occipitalcondyleandauditorybulla,
Lycalopex is the only genus that is not monophyletic, we shorter and thicker muzzle, small first molar and larger
alsoincludedtaxonomyinitsmodel.Theothergenerawere carnassial, canine and incisors.
not analyzed separately due to low number of localities. MANOVAperformedusingthefirst25RWsevidenced
significant shape differences between species (N = 262,
Comparative Methods Pillai’s trace = 4.116; F = 13.471; P (cid:3) 0.001).
175, 1652
When only locality average sexed individuals were ana-
Skull size and shape values together with bioclimatic and lyzed(N = 206),two-wayMANOVAshowsnosignificant
competition parameters were averaged across species in differences between sex (Pillai’s trace = 0.173;
order to identify correlation patterns at macroevolutionary F = 1.385; P = 0.118), but confirms significant
25, 165
(above species) level. differences between species (Pillai’s trace = 4.146;
Thisnewdatasetincludedeightdatapointsonly.Wetested F = 9.936; P (cid:3) 0.001), with no interaction
175, 1197
again for allometric patterns in between species as well as between the two factors (Pillai’s trace = 0.895;
impact of climate and competition using Partial Least F = 1.003; P = 0.477). Pairwise comparisons
175, 1197
Squares.Duetospeciessharedancestry,wefirstlyproduceda using the first two RWs (50.46 % of total variance)
molecularphylogenyofourselectedtaxausingthe10 ktree revealedthatallspeciesdifferinskullshape,expectforthe
projectdatabase(Arnoldetal.2010,OnlineResource).This pair Lycalopex culpaeus–L. griseus, L. culpaeus–L. gym-
database provided access to all updated molecular data of nocercus and Atelocynus microtis–L. vetulus (Table 2).
extant Canidae and generated consensus phylogenetic tree
basedonabayseanapproachusingselectedtaxaonly.Mor- Skull Size
phoJwasemployedtotestforthepresenceofaphylogenetic
signal in our shape data comparing the observed sum of Two-wayANOVA(N = 206)revealedcanidspeciestobe
procrustes distances between the eight species averaged significantly different in skull size (F = 123.069, df = 7,
shapes and their reconstructed ancestral node values versus P (cid:3) 0.001). Males and females also differ in skull size
thedistributionofthesesumsobtainedrandomizingtipsand (F = 7.946, t = 1, P = 0.005) but no interaction occurs
nodevalues(cf.KlingenbergandGidaszewski2010;Meloro between taxonomy and sex in skull size (F = 1.057,
and Jones 2012). Regressions and Partial Least Squares df = 7, P = 0.393). Therefore, it was possible to use in
models were eventually repeated on independent contrasts subsequentanalysesthelocalitiesaveragesincludingthose
using MorphoJ in order to re-evaluate the influence of individualswholackedsexinformation.One-wayANOVA
allometry, climate and competition on macroevolutionary confirmed species to be significantly different in size after
scale(cf.Meloroetal.2014a,b). averaging by geographic localities (F = 194.9, df = 7,
P (cid:3) 0.001). Paired comparisons revealed that all species
differinsize,exceptthepairA.microtis–L.culpaeusandL.
Results gymnocercus–S. venaticus (Table 3; Fig. 4).
Canids Skull Shape Skull Allometry
The first twenty five Relative Warps cumulatively explain Sizehadasignificantimpactonskullshapeexplaining7.84 %
95 %oftotalvariance.Plottingthefirst(30.50 %ofshape ofvarianceintheglobalskullsample(N = 431,P (cid:3) 0.0001,
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EvolBiol
Fig.3 Scatter plot of RW1 versus RW2. Transformation grids accordingtodifferentcolorandsymbolwithinminimumconvexhull
visualizeshapedeformationsrelativetothemeanatthepositiveand superimposed(Colorfigureonline)
negative extremes of Relative Warps axes. Every species is labeled
Table2 PairwisecomparisonsbetweenSouth-Americancanidspeciesforskullshape
A.microtis C.thous Ch.brachyurus L.culpaeus L.griseus L.gymnocercus L.vetulus S.venaticus
A.microtis 0.008 (cid:3)0.001 <0.001 (cid:3)0.001 (cid:3)0.001 0.275 (cid:3)0.001
C.thous 4.924 (cid:3)0.001 (cid:3)0.001 (cid:3)0.001 (cid:3)0.001 (cid:3)0.001 (cid:3)0.001
Ch.brachyurus 29.160 45.111 (cid:3)0.001 (cid:3)0.001 (cid:3)0.001 (cid:3)0.001 (cid:3)0.001
L.culpaeus 40.531 41.745 34.926 0.107 0.142 (cid:3)0.001 (cid:3)0.001
L.griseus 38.199 150.730 115.400 2.472 (cid:3)0.001 (cid:3)0.001 (cid:3)0.001
L.gymnocercus 15.378 126.780 63.463 2.0208 14.211 (cid:3)0.001 (cid:3)0.001
L.vetulus 1.6110 28.661 84.289 43.912 67.453 48.654 (cid:3)0.001
S.venaticus 67.480 496.61 447.590 205.290 410.350 390.020 107.510
UpperdiagonalcorrespondstoPvaluesandlowerdiagonalcorrespondstoFvalues.Significantishighlighted
Table3 PairwisettestbetweenSouth-Americancanidspeciesforskullsize
A.microtis C.thous Ch.brachyurus L.culpaeus L.griseus L.gymnocercus S.venaticus
C.thous 0.002
Ch.brachyurus (cid:3)0.001 (cid:3)0.001
L.culpaeus 0.488 (cid:3)0.001 (cid:3)0.001
L.griseus (cid:3)0.001 (cid:3)0.001 (cid:3)0.001 (cid:3)0.001 (cid:3)0.001
L.gymnocercus (cid:3)0.001 (cid:3)0.001 (cid:3)0.001 (cid:3)0.001 (cid:3)0.001
S.venaticus (cid:3)0.001 (cid:3)0.001 (cid:3)0.001 (cid:3)0.001 (cid:3)0.001 0.140
L.vetulus (cid:3)0.001 (cid:3)0.001 (cid:3)0.001 (cid:3)0.001 0.043 (cid:3)0.001 (cid:3)0.001
SignificantPvalueishighlighted
seealsoOnlineResource)and9.46 %ofvarianceinthelocality Allometric models using pooled regression within subgroups
averagedsub-sample(N = 262,P (cid:3) 0.0001,seealsoOnline are also significant in all cases (N = 431, 3.29 Var%,
Resource).ANCOVAmodelswithpermutationdemonstrated P\0.001;N = 262,3.77 Var%,P\0.001).
in all cases that slope differ between species (N = 431, Regression models performed independently for each
F = 8.713, P\0.001; N = 262, F = 1.872, P\0.001). taxon (Table 4) demonstrates that allometric effect impact
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EvolBiol
Fig.4 Boxplotwith
standardizeddeviationof
naturallogtransformedcentroid
size(lnCS)acrosstheSouth-
Americancanidspecies.Black
stringmedian,whiteboxfirst
interquartile,barsecond
interquartile
Table4 Regressionsbetween
Species Wholesample Localityaveraged
skullshapeandlnCSin
differentsubsamplesofcanid N Var% P N Var% P
taxa
Cerdocyonthous 226 3.85 <0.0001 143 4.08 <0.0001
Chrysocyonbrachyurus 25 9.28 0.0076 19 11.52 0.0159
Lycalopexculpaeus 13 10.85 0.835 7 25.85 0.0731
Lycalopexgriseus 33 4.86 0.1003 19 7.19 0.1881
Lycalopexgymnocercus 99 4.20 <0.0001 55 5.69 0.002
Lycalopexvetulus 16 6.68 0.4329 7 26.71 0.0865
Lycalopexspp. 161 9.13 <0.0001 88 9.02 <0.0001
Speothosvenaticus 15 13.44 0.0346 10 20.81 0.0084
Significanceishighlighted
species differently. In the bush dog skull size explains the Seasonality (standard deviation 9 100) (BIO4,
highestpercentageofshapevariancewhencomparedtothe r = -0.864) and Temperature Annual Range (BIO7 =
larger Chrysocyon and Cerdocyon. Within Lycalopex BIO5–BIO6; r = -0.762), while strong positive correla-
allometric shape changes occurs in L. gymnocercus only tion of SW1 climate scores occurred with Annual Mean
while they are not statistically detectable in the other taxa Temperature (BIO1, r = 0.864), Min Temperature of
(see also Online Resource). However, if all Lycalopex Coldest Month (BIO6, r = 0.943), Mean Temperature of
species are merged inthe same sample, skullsizeexplains Driest Quarter (BIO9, r = 0.794), Mean Temperature of
almost9 %ofshapevarianceinbothcompleteandlocality Coldest Quarter (BIO11, r = 0.931), Annual Precipitation
averaged datasets (Table 4; see also Online Resource). (BIO12, r = 0.809), Precipitation of Wettest Month
(BIO13, r = 0.891), Precipitation of Wettest Quarter
PLS Climate (BIO16,r = 0.896).Therefore,SW1climatediscriminated
betweenseasonalandaridclimate(negativescores)versus
Two block Partial Least Squares between 19 bioclimatic warm and humid (positive scores).
variables and skull shape extracts 19 pair of vectors of Species distributed in localities with low precipitation,
whichthefirstexplains98.33 %ofcovariationbetweenthe low mean temperatures and high seasonality exhibited
blocks. Correlation between the first pair of axes is strong skulls with elongated muzzles, smaller zygomatic arch,
(r = 0.720)andsignificant(P\0.001).Ascatterplotwith larger teeth, narrow auditory bulla and smaller occipital
Singular Warp 1 of the shape block (SW1 shape) versus condyle (e.g. L. griseus, L. culpaeus and most of L. gym-
SW1 of the climate variables block supports a separation nocercus representatives). Conversely, A. microtis, S.
among species along an environmental gradient (Fig. 5). venaticus,L.vetulus,Ch.brachyurusandmostofC.thous
SW1 climate is loaded negatively on Temperature representatives showed positive scores in vector SW1
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EvolBiol
Fig.5 PlotofthefirstpairofSingularWarps(axisXisblockshape, scores. Every species is labeled according to different color and
axis Y is block climate). Below deformation grids and variables symbol within minimum convex hull superimposed (Color
profile from the most negative to the most positive Singular Warps figureonline)
climate (high precipitation and mean temperature and low groupsofspeciesthatdifferamongeachotherthemost:the
seasonality) and therefore had antagonistic skull shape northern group, with A. microtis, most specimens of C.
(Fig. 5). thous, Ch. brachyurus, L. vetulus and Speothos and the
ThePLSofsizeversusclimaticvariablesalsoextracted southern group, with mainly L. griseus and L. culpaeus.
a significant pair of axes whose correlation is not particu- Lycalopexgymnocercusisrightinthemiddle,overlapping
larly strong (r = 0.275; P\0.001). SW climate is loaded in shape with both groups (Fig. 7). SW1 competition is
positively with Temperature Seasonality (standard devia- loaded positively with all three variables (Diet r = 0.823,
tion 9 100) (BIO4, r = 0.827). All Lycalopex species Interspecific killing r = 0.578 and habitat r = 0.572).
occur in high seasonal environments and are characterized Adaptationsinthepositiveend(L.griseus,L.culpaeusand
by relatively small size (Fig. 6a). L. gymnocercus) are related to skulls with a larger bulla, a
small temporalis insertion area and relatively larger teeth.
PLS Competition On negative scores we find specimens of C. thous, Ch.
brachyurus, L. vetulus and S. venaticus. These specimens
Two block Partial Least Squares between competition show relatively smaller teeth, bulla and larger muzzle.
variables (Diet, Size and Biome) and skull shape extracts Significant association also occurs between size and
threepairsofvectorsofwhichthefirstexplains70.97 %of competition (r = 0.332; P\0.001). SW competition is
covariation between the blocks. Competition has signifi- loadednegativelyondiet(r = -0.662),size(r = -0.036)
cantimpact onskullshape(PLS1,r = 0.419,P (cid:3) 0.001). and biome (r = -0.748). Species with higher impact of
The scatter plot with Singular Warp 1 of the shape block competitionaresmaller(L.griseus)andwithlessimpactof
versus SW1 of competition variables block shows two competition are larger (Ch. brachyurus) (Fig. 6b).
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