This article isprotected rights by All copyright. reserved. 10.1002/ecy.1910doi: lead todifferences version between this andthe ofPleasec Version Record. been and throughtypesetting, proofreadingwhich may thecopyediting, process, pagination This article undergone has for and buthas accepted been not review publication fullpeer USA 8 USA CA, 7 Universidad de Complutense Madrid, Spain 6 5 4 3 2 1 Maria EspeltaJosep Guille Peguero Articletype : Articles
Department of Global CSIC, DITEG University Group, Castilla Research of Forest Research(GIF),INDEHESA, GroupSpain Extremadura, University of CREAF, Cerdanyola Vallès, del Departamento de de lasCienciasFacultad Didáctica Experimentales, de Educación, AcceptedInstitute and ofthe Sustainability, Environment University California,Los CA, of Angeles, Article
Cerdanyola del Vallès,Cerdanyola del EcologyUnit CREAF Tropical insect diversity: evidence of greater host specialization
1,
2 Ecology andLosEcology Evolutionary Biology, California, Angeles, University of , 9 , Raúl Bonal 2
- 3,4 CEAB 08193 , in in seed 08193 Dani
- Catalonia, Spain Catalonia, CSIC el
Catalonia, Spain
- Sol feeding
- 2 UAB, Cerdanyoladel Catalonia, Spain Vallès, ,5
, Alberto Muñoz - La Spain Mancha, weevils
2, 6 , Victoria L., Victoria Sork
ite this articleite this as
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This article isprotected rights by All copyright. reserved. weevil local andregional level. weevils in numbersHill ofeffective oak relationships species level pool of in temperate and tropical the hypothesis a in radiation hypothesis lacks to specialization estimations, and thedifficulties toseparate thediversityattributable component proved challenging beca diversity insects thetropics. ofphytophagous However, in addressing hypothesis has this A LeeCorresponding Editor: A.Dyer ManuscriptAprilMarch 2017; received 27 27 2017;revised Running head: Department, Belgium Antwerp, 1,Wilrijk, University of Universiteitsplein Present address: 9
CorrespondingE Author. bstract
Acceptedinsect Article - weevil food webs and and foodweevil webs
s oak host pecies specialization from that related diversity. tohost aspeci result, thehost As . Nicaraguacompared richness toCaliforniasimilar species despite at ofhost both Host specialization has theextraordinary long toexplain beenHost specialization hypothesized
778 weevil larvae 778 weevil by
were Specialization inseedSpecialization
M Center of Excellence of (PlantandCenter PLECO Biology Vegetation Ecology), species. empirical aximum aximum highly specialized use of the risk ofover B Using regions species. y means of - examined support for important phytophagoussupport for important clades. insect mail: [email protected]: L
of seed ikelihood extracted seeds from host DNA DNA
(California and Nicaragua,(Californiaand with respectively)
We foundalpha,We gamma a and diversity higher beta of
-
feeding insects, acornfeeding insects, ( weevils - differencesgamma alpha,and betadiversity in sequences from threesequences low from Bayesian mixed models Bayesian mixed feeding insects
and Bayesianand inference. We both in termsboth in range ofhost and interactionst - looking rarelooking interactions,
and
acceptedMay 10 2017. , assessed assessed
we - copy genes, wegenes, to copy delimited also then reconstructedthen Curculio spp Curculio their phylogenetictheir found thattropical and henceand
Here, w
an equivalent .), sampled
biasing alization alization rength, using using
e
the test
This article isprotected rights by All copyright. reserved. interactions importantprocessesgenerating evolutionary trigger ecological should diversity, (Dobzhansky2014) et al. 2009,Brown 1950,Schemske environmental biotic interactions stability theimportanceof abiotic stress increase over tropicalenhanced regions their greater benign if productivity, climatology, more and havefor proposed.is been instance Resource specialization partitioned inthe tropics thanintemperate species more reducing finely and partitioned, niche facilitating thus overlap coexistence of many expected inthetropics Ahighdiversity isnonetheless ifresources individuals. are either a ofa diversity high composed individuals ora relativelyfew lowdiversitycomposed 2014) productivitymore mayviable thetropics species allow populationsin tomaintain this widelymost recognizedandof fascinating life. Nowadays, isagreement patterns there that The increasing gradient latitudinal from isone of the polestothe biodiversity tropics I phylogenetic MCMCglmm Key temperateregions absence h evendifferences in in of specialization hypothesis relationshipthis was absent. acorns be specializa expectedhost greater as by infested, would a Finally, was larvalsize body inNicaraguanspecies, highly ofthe correlatedwiththe size whereas their Accepted ArticleNTRODUCTION - pattern words: words: . However, thisex (Hutchinson 1959,Brown(Hutchinson 2014) is in partto is in due b eta diversity temperate
planationinsufficient is canecosystem because a support productive congeners
andeco suggest contrasting ; ;
Curculio phytophagous insects an increase
Altogether had ; insect
a broader taxonomic and phylogenetictaxonomic spectrum host a broader , these in productivity towardin productivity the . The reasons why. The be reasons should more niches finely regions regions - plant interactions plant lines ofevidence support lines ; Quercus remain some hypothes unclear, although ost diversity - evolutionary dynamics intropical dynamics and evolutionary . A
.
predominance of bioticpredominance of
expected to be more common in expected tobe ; latitudinal latitudinal diversity . tion, whereastion, inCalifornia
tropics
the host host the , as ahigher, as among (Brown
gradient of
the e ; . s
This article isprotected rights by All copyright. reserved. tropics mediated is by the the E al. 2010,Foristeret al.2015) as seed however,among insect differ we guilds and generally comparative recentlyanalysis has compelling evidence provided thatphytophagous insects specialization sampled, which Schleuningal. 201 et controversial sofar of phytophagous insects thetropics in Despite 2014) the preponderance ofbiotic interactions underlyingwould be thekey thetropics in mechanism According hypothetical tothis model, therefore,ecological driven specialization by a rangesturnover spatial and higher of populationssubdivision conducive as tospeciation, well asdistribution lead tosmaller al. 2006,Salisburyal. 2012,García et features, 2014) (Schluter 2000) including character displacements,
Acceptedvidence Article
t gradient diversitylatitudinal of heory . .
Lo -
feeding insects host specialization has long been hypothesized to explain theextraordinary specialization hastoexplain host long hypothesized been diversity
such as mountain rangessuch as mountain wer abiotic stress should reduce should werabiotic stress thermalgeographic tolerances, species’ making for the host specialization hypothesis the only specialization not host for is insufficient, diet breadths latitudes narrower have atlower
require further attention. Onerequire further is (Ollerton and , and should also , and should may (Ollerton andCranmer(Ollerton Novotnyal. et 2006,Dyer 2002, etal.2007, 2) lead toover lead , which otherwisegeneralize to would help thosefindings . One importantthattropical reasonis be regions tendto richness Cranmer 2002) .
- prevent by niche shifts , look ra
(Janzen 1967,Ghalambor(Janzen Brown 2014) et al.2006, stronger barrierstodispersalstronger of adaptive radiations andadaptive radiations co (Schemske et al. 2009,Salisbury et(Schemske Brown al. et al.2012, - host species species host (Lewinsohn and Roslin 2008) and(Lewinsohn Roslin Robledo et al. 2016) etRobledo re interactions andhencereestimates interactions of bias the extent towhich the extent . Despite . Despite still still lack information from (NovotnyLewinsohnet and al.2006, the (Forister et al.2015) enhanc difficulties, a globaldifficulties, a
. This in turn should favor genetic turnshouldfavor. Thisin -
evolutionary the ing (Janzen 1967,Ghalambor(Janzen et
higher specialization in the higher specialization
biotic resistancebiotic , evidence been have
but important groups such important crucial aspects of dynamics . Diet breadths, - wide insufficiently
(Novotny et
( Brown . This article isprotected rights by All copyright. reserved. Acceptedof seed pool ofpotentialavailable. hosts comparisons ofinse gradually decreases poleward with a of160 Mexico, does butin peak not maximum inthe equator groups phytophagous of insects, theradiation oak ( hosts oftheir genus with specialized long usedtodrillholes inseeds primarily noses ofa oftrees, variety ofthe weevils ( through insect study a of Here,we in tropical regions. higher host et al.(2015) Article(NovotnyLewinsohn 2008) et and al.2006,Roslin specialization from host component attributablethat related to gradientlatitudinal of biodiversity also offerstrong but would the hypothesis supportfor specialization does differhosts not fromthat foundintemperate regions. diversity ofphytophagous if resource specialization consumer tobefinely more partitioned regional and level local 2008) Roslin Quercus - feeding hasbeen insects previously highlighted Curculio, Curculio, investigate
diversity contribute diversity addressed this .
T is higher thetropics regardless in of
(Gibson 1969,1977) (Gibson ropical regions usually
Curculionidae, Coleoptera).Curculionidae, Direct evidenceDirect lacking. isnonetheless ct
the importance of host specialization inthe latitudinal the importance ofhost specialization diversitygradient - plant associations within a associations within singleplant constant radiationwhile keeping the ,
and - host associationshost thestriking in ofacornradiation evolutionary is
insects
issue driven by interactions
it isoften it (Nixon 2006) (Nixon s
but does not fully but doesnotfully indirect While the While
in the tropics . Hence, , inorder toforage and
believed harbor harbor (see Forister(see etreferences therein) al.2015,and ly t by means ofpath analysisby means
. Thisallowsconducting tropical he he importance inthe diversity ofhost specialization a higher diversity of potential host plantsat a diversityhost a ofpotential higher challenge is to bechallenge isto able toseparate
Acorn weevil adults areAcorn poorly flying in may that this this that
betweencompeting host host . explain thehigherexplain
In their still still
a new tounderstand perspective richness (Janzen 1980) (Janzen would occur
Demonstrating that Demonstrating lay their eggs. Unlike other their eggs.lay comprehensive comprehensive
to
even when the diversitywheneven of allow the niche of the would not only providewould not Quercus differences diversity inhost - 165 species, and
; they specialization , its contribution to the contribution to , its insects genus, L.,genus, 1758) showed analys - , a higher temperate dietary the diversity i s, Forister s,
that of insects the . sects a Yet
This article isprotected rights by All copyright. reserved. Acceptedindex ofhost dimensions the their phylogenetic purpose, Tothis we relationship. constructeda phylogeny molecular all for aexhibiting higher inthe tropics thanintemperate irrespective hostspecialization regions of Therefore,whethe asked we was higher inthe tropical estimated theregional ofspeciesgammaconfirmed thatalpha, and pool beta diversity 2014) providing insect undisputed species to delimit level weevil larva YuleGeneralized Coalescent Mixed basedinformation to models (GMYC) onmolecular latitude (California)another and (Nicaragua) tropical exhaustively weevils biogeographical acorn intwo sampled regions ArticleTo investigate allowing gap this tofill species biogeographicall evolutionaryand for ecological group informationthis skewed available is severely phylogenygenus the any of lack species ofthese species region for whole Neotropical the acorn are no weevils particularly life immature stages, for i gradientlatitudinal Incomplete been ofnever evaluated. diversity has knowledge, taxonomic
species regions,and sampled used phylogenetic inboth
. d’
Once species weevil from the Nicara -
level delimitations without formal without morphological delimitations level descriptions contain a regional similar poolofoak species -
between Additionally, theseregions. andtemperate tropical by means whether y.
Notwithstanding, Notwithstanding, specialization t an
. host specialization affects specialization the latitudinal diversitygradient,host we
exception. Todate, one theremonographis just describing 27 region - r the observedcould patterns beexplained byweevil species host associationshost (Nicaragua) than - host range,host interactionstrength and e
DNA sequences from specific genesDNA from sequences today specific enables rearedfrom acorns, t incubated s arguably the main barrier to gatherings arguably mainbarrier to the and such data (Gibson 1977) (Gibson gua California wereand well characterized, we -
(Pinzón which (Hughes 2004a) and Vogler
in the
despite their remarkable differencedespite their remarkable in - (Nixon 2002,2006) (Nixon Navarro et al. 2010, Muñoz etNavarro al. Muñoz et al.2010, , and comprehensive themost
temperate
- based methods to compare methodsto based three
one - hus additionally one temperate the (Pons etal. 2006)
(California) region. . specialization specialization First, w . Hence, the
of e used ,
thus This article isprotected rights by All copyright. reserved. diapause. and fina 2008) Munoz the seed coat (Gibson 1969,1977) families Thegenus the species of Study group M be tighter thanintemperateregions. inthe tropics et al al. 2011) acorns bodyexploit size ofdifferent adaptations size to plausible thatmuchof of weevils theinterspecific diversification may been have triggered by andadult size future fecundity becauseend strongly bodyatof is larvaldevelopment size the relatedwith larval survival, growth single, sometimes multi acorn and bodyThe size weevils’ size. larvae of possibility thatspecialization evolution ofhostspecializationinthese insects. S phylogenetic
AcceptedMETHODS AND ATERIAL Article . 2009) (Bonal and Munoz 2008) (Bonal and Munoz , lly emergelly topupate, and inthepassing burrow topsoil by the unfavorable seasonin
. If. interactions the ofbiotic strength varies beingFagaceaeandgenus particularly the
, the expectation is that thecorrelation is between, theexpectation and should acorn larvalsize size
- with their specialized long rostrum, . Larvae. the inside acornsfeedingduringendosperm develop onthe 2 based methods we thatmay also methods assessedbased mechanisms influenced have the . After mating,. After weevil select females a - infested seed, and the lack ofresourcesinfestedand seed, severely thelack can restricttheir Curculio Curculio
might (Desouhant etal. 2000 . This (Coleoptera, Curculionidae) feed onseeds be associated constraint Curculio where econd may consequences important have fitness with
Quercus
along gradient latitudinal the , Bonal etal. 2012) differences between intherelationship , we (Hughesand 2004b, Bonalet Vogler they
complete their a development in host tree and drill ahole treeandhost drill specifically their most common hosts hosts common their most lay lay their eggs examined the . It istherefore.
(Bonaland
of various plant
(Schemske - 4 weeks4 through This article isprotected rights by All copyright. reserved. Accepted Autónoma de Nicaraguaat by plant field and found inaccessible branches. punctures duringcoat weevils intheseed Adult wereby oviposition. when up hand picked Infestedinfestedacorns acorns. branches available focal actively trees of three and search then people sites. Forsampling atgently 60minutes methodacross eachwe sampling site,shook 2009) forSeptember Nicaragua and(2010)for Califor during ofthe most oak ripen species inwhich their theperiod acorns: July rangingfrom 600 landscape Articlepresent ateach (Fig. region 1,Supp more than 58.000km andCalifornia 17sampling and Nicaragua sitesin indicating that incl represent different evolutionary lineages (Stevens Nicaragua, richness comp where is theoak Our Study areas method andsampling ude representativesthe red (sect. of oak
study was conducted inthe Centralstudy ValleyCalifornia conducted Las was and of region Segovias in experts et al. identifications werefurtheridentificationsconfirmed wa s a mosaic ofs amosaicpasture circums oak woodlands and
2001; Nixon2002) the phylogenetic spread of potential hosts is also is comparable. We selected hosts the phylogenetic spread ofpotential 29
from - 1800 m 1800 2
U and covering thus range thedistribution ofthe oak ofalmost species all niversity of California at Los Angelesniversity ofCaliforniaat
a.s.l. California800 in and León The oak host species The oak species host were .
. Quercus orting
easily (Nixon 2002) (Nixon
information arable with 20and16species,arable respectively Lobatae distinguished by the black dots resulting the distinguished byfrom dots theblack is a large genus whichis alarge insections divided bycollecting p ,
respectively, sampli were ) and (sect. white oak -
1700 nia. Westandard used thesame Appendix Appendix . California and Nicaragua both
identified by visualinspection inthe identified
m
in Nicaragua. sampled We and U cribed to an altitudinal belt altitudinal cribed toan lant material material lant S 1, Table niversidad Nacionalniversidad ed ng over anng of area
the groundfallen for the - Quercus August (2007 S to beexamined 1). The ) sections, ) sections, - This article isprotected rights by All copyright. reserved. reducemissing proportion data. of the Corp., AnnArbor, The sequences USA). were trimme Sequencechromatograms wereassemblededited and using B Sequencing stran both wasfrom done proceduresPCR inHughes& described ( Vogler ofgene thenuclearfactor elongation ( 1α 3014 ( I subunit oxidase ( protocol from of a2mmcaudal portion each(abdomen forsalt extraction adults) following larva a used a procedure speciesdelimitation under possible ais not W Nicaraguaany match the didnot described species in of 1927), identified abundances treeall host samplingand species all sites alla sitesand all representativeoak species,we subset selectedweevillarvae of coming from ceased preserved plasticand vialsfilled with95 in1.5ml each larva was of light/dark, temperatureLarval and humidity. emergencedaily was monitored it until Infestedtrays individuallyconditions acorns wereconstant inplastic under placed inthelab Species andphylogenetic delimitation reconstruction IG
Accepted eevil larvae Article D YE LoxdaleLushai,& 1998) C. occidentisC.
2.1 and an ABI PRISMan ABI3730analyzer2.1 and (AppliedBiosystems, USA).Foster, (Aljanabi 1997) andMartinez
some adult specimens from California as some adult from specimens as California in the field
do not present diagnosticstructures, organsor do notpresent sothat cox1 (L., 1758) and(L., classic morphologicalclassic
) and cytochrome) B ( (see Appendix S1 for S1 s (see Appendix , and CB1 and CB2 and, and CB2 CB1 C. aurivestisC.
ds with the same primers used for the PCR using thesameds with primersPCR for used the
based onmolecularbased information . We amplified. We the mitochondrial cytochrome genes EF1α by cytb
balancing their numbers in proportion to the to inproportion balancing their numbers framework ample sizes). Following sizes). ample ) using the primers EF1) using theprimers
) using) theprimers C1 2004a) (Chittenden, 1927). Adultspecimens(Chittenden, from belonging to (Simon et(Simon al.,1994)
d to711,413and581base pairs to
. To Gibson (1977) were threegenes. for followed the
S circumvent this hindrancecircumvent this w EQUENCHER EQUENCHER Curculio pardus pardus Curculio
taxonomic classificationtaxonomic . - . - Gibson (1969) Gibson DNA wasDNA extracted R and EF1and R , J
% ethanol. - and also afragmentand 2183 and L2 and 2183 4.6 (Gene4.6 Codes (Chittenden - F. The
To , - we N obtain - e c
This article isprotected rights by All copyright. reserved. Accepted1000 steps. Standard convergenceMarkov checked diagnostics chain were that toensure 2012) (Guindon etal. 2010) assess therepeatability the topology of likelihood and the ML with analyses were performed of tree andthe topology thestrength nodes were of InformationAkaike Criterion (AIC) using then concatenated.Best 2004a) Curculio and To establish the phylogenetic relationships species, sequences amongweevil the ( preliminary numberseach asoperativeof for thespecies names Articlecorresponding with packagein the R (Hughes 2004a) and Vogler PAUP* model withRAxML 7.0.4 abuild Maximu (Pons etal. 2006) to speciation patterns This model tracks tree ratestransitions from(intra coalescent identifying branching GMYC modelswere EF1α those of
applying two parallel Markov chain runs of two million generationsapplyingtwo million Markov chain twoparallel every sampling runsof . The three genes weregenesaligned. Thewith threeseparately
4.0 species and again with species with and again ) of onegroup per) of individual GMYC pooledwith 15additional temperate were (Swofford 2003) the Linnaean m Likelihood (ML) SPLITS adult . After identical. After collapsed, haplotypes were we used , then then . Bayesian. analyseswere performed with
thereby delimiting independentlymtDNA clusters evolving lineagesor species -
(Pons et al.2006) (Pons fit modelsofnucleotidefor each substitution genefit wereassessed by names. ForNicaraguan however,we specimens, used to delimit speciesused to delimit (Stamatakis 2006) . The GMYC analysis. Thewas GMYC done withthe ‘single , using
previously identified, sothatpreviously we assign identified, were able to themtheir C. pyrrhocerasC. RAxML 7.2.6
the gall feedingthe phylogenetic .
J Thea sequences of M . The . The ODEL set asan outgroup
- tree applying substitution a GTR+I+G (Stamatakis 2006) (Stamatakis level entities p T assessed hylogeny Curculio pyrrhoceras Curculio EST C LUSTAL
0.1.1
- ra
tio testofbranchtio support by
was madewas with ultrametric (Posada 2008) ll Californian larvae Californian ll matched M based on - W ML level delimited. entities R
(Larkin et al.2007) .B (Hughes and Vogler , and and Bayesianand inference. AYES AYES all identified species
the the
P had touse had as outgroupas 3. HY - cox1 2 . The reliability threshold’ option ML
(Ronquist etal.(Ronquist
haplotypes. haplotypes. cox1 was usedto - spec
and , cytb ific) ific) s
to , This article isprotected rights by All copyright. reserved. sampling sites. were by at supported least supported by two observations one just or confound et al.,200 Quercus To assess differencesspecialization of host weevil among in regions species,quantitative subset of sites(parameters ineach were 10sites from region). 100samples nestedness 2012) turnovercomponents andwith nestedness ( the ratio ofwee richnessweevil anddiversity of of(2) species, oak number per hosts Kruskal raref inverse concentration ofSimpson 0),= Shannon diversity1,exponentialofShannon(q entropy) and diversity = Simpson 2, (q used To measures Diversity andhostspecialization burn reached were the‘all stationarity. Trees summarizedusing β
Accepteddiversity) bywas ofS assessed means Article test for - actionextrapolation and asymptotic in (Appendix in (Appendix . Thisprocedure 3multiple computes - - Wallis tests were tests thenused (1)Wallis among toassessin regions differences Curculio Curculio ing 8)
- differences in local andregionaldifferences diversity ofweevil species in resultant fraction fraction resultant ,
following framework the specialization withrarity
vils per host. Variation in the composition of weevil Variation per assemblages intheamongvils composition sites host. diversity estimates diversity trophic webstrophic were drawn S 1, Figure 11
β
procedure trophic interactions S ne 1).
and overalldiversity beta ,
Jost 2006) Jost
based numbers onHill , w , described ,
using the R packageR the using ørensen index e
( the R excluded excluded - Novotny et al., 2012) Novotnyet
s by means of by means ite dissimilarities (species turnover
were calculated with - package in in recorded Novotnyal. (2012) et 3
Nicaraguan species ,
which was
‘betapart’ the R - ,
in of q order 25% with consensus compatible’ β sør ‘ a minimum ofsix a minimum iNEXT - package package themforand a resamples ) . The rest of interactionsThe of rest
a sample partitioned into its speciespartitioned its into (Baselga and Orme . S sampling sampling ’
between (Hsieh et(Hsieh al.2016) pecies richnesspecies = (q ‘bipartite’ .
To avoid To which -
size site, and (3) site, and (3) local species
region different
β - were based tu
(Dormann
, , we we . This article isprotected rights by All copyright. reserved. Accepteddevelopment,growth was oriftheir restricted byavailability. for resource each weevil Then, to discern if fed larvae had with aprolateEach spheroid. acorn w measured withadigitaland caliper equivalencegeometric their volume derivedassuminga each rearing species.After weevil width andlength larvae,all theacorns were the of larval size body prediction, notdiffershould different among inthemore hosts generalist weevil oak Totest species. stronger i expected betweenIfdifferences therewere significant specialization inhost Morphological differences between andtemperate tropical weevils than one weevil ranges host Articlesectionsa was rough as recorded measure ofphylogenetic specificity whether toassess specialization availabilityeach of host sampling of to o specialization index host with the reared ( rangehost consideredWe many ofinsect dimensions threeofthe host ak host
relative toall interactionsrecorded, Foristeret al., 2015 ir oak n theregion where betweenthe relationship
main host (i.e.main host the between proportion ofweevil interactions aand species main its
as
we assessed the relationship between the width oflarval relationshipwe the between the (i. assessed head availability available
genus sections (Appendix (Appendix genus sections the number ofoaklarvae fromgivenspecies hosts a which the number weevil of ). Additionally,affiliation theof
and adult fitness and adult were d’ interacting partners , which expressesa how given specialized weevil relation isin species
, bycalculating
restricted to closely related speciesrestricted toclosely oralternatively related of one ofmore t h e ). Second, we estimated theinteraction). Second,estimated we strength ad libitum
host index index , - specificity Bonal etal., 2011) the size of the size d’
, i.e.there endosperm was they left when finished their ranges0 (no specialization) to1(perfect from as toassess dissected the remaining inorder endosperm the extent towhich the extent S Bascompte et al.,2011) 1, Table (Blüthgen et al.2008) (Blüthgen
was higher. weevil weevil Quercus S 2).
and the andacorns thevolumeof the by infested
species to This is becauseThis is
a deviatesfrom species arandom - specificity. First, weFirst, measuredspecificity. acorns they infest . . Third, we . Third,we W Lobatae Lobatae
the studied regions eight
ed larval performancelarval or
of insect species e. a proxy of by theoverall measured Quercus ed
to ha
be d
, the
we been been this this This article isprotected rights by All copyright. reserved. Accepted(phylogeny) / was index (Hadfield 2010) and means ofHeidelberg informative prior used was Poisson, models with recorded of interactions weevil between relative a and speciesmainhost its toall interactions (1969) species data with published information relationships.To increase structures Article(Hadfield 2010) Markov chain Carlo Monte temperate To Phylogenetic which they had emerged information oft measuredimagingcoupled withasoftware ( stereomicroscope ( species investigate in differences
by .
ensuring a ( To model variation in host range inhost To model variation ofhosts),interaction (number strength ( henceforth ) and nd sites as weevil species weevil assessed
random effects random - based [ the the variance he head of
. . Phylogenetic signalhostrange, interaction of strength , a subset oflarvaegrown , a subset that These specialization index specialization M
by referred asreferred temperate or comparative methods - the OTIC Welch Binomial calculating thephylogenetic heritabilityas each variance trait of
type ( , autocorrelation for phylogeny) + ,
59 from California and
sample size we fitted DM 178
in allcases. C (MCMC)
s
in linear models, including tests
traits related specialization tohost of models of - larvaecorrespondingacorns and the from volume ofthe
143, Xiamen,head China) andcapsule was thewidth ofthe and Gaussian
of range host
(to ass phylogeneticgeneralized , as implementedintheR
and phylogenetic breadth d’ variance (residualvariance allow ess c that chains
onvergence diagnostic of chains waschainsonvergence checked diagnostic of by (log
ad libitum ad libitum both fixed M Near
-
distribution transformed), we respectively we transformed), of to explore to explore OTIC OTIC
eight additional c 119 119 tic species tic I MAGE MAGE was photographed with adigitalwas photographed with from Nicaragua.
and those arising from phylogeneticthose arising from a ) the inclusion of complex covariancethe inclusionof complex
me from a distribution) me from stationary ] of errors
P random effects (HadfieldNakagawa and 2010) LUS linear indistinctly - , we complemented, we our own package between
2.0). North American . A general non . A mixed models mixed We obtained obtained We
and
‘ ) tropical tropical MCMC
from Gibson from was kept below0.1
specialization implemented the number the number and glmm’
- Curculio Curculio based on
.
This article isprotected rights by All copyright. reserved. wereanalyzed, for when separately each species weevil of possible, bylinear means models performance inoak developed belonging when hosts todifferent grown Nicaragua and California. acornclearly separatelyran onlybetropics, volume should we models observed inthe 2014 we species includedand identityas factors phylogeny random in 2) phylogenetic amongclose autocorrelation auto analysis larval ofand theacorns head thevolume W we ran for 1000simulations each trait thepackage using ‘phytools’ Lapiedra2003, et al.2013) phylogenetictransitions on branchesa process under Markov evolution of Carlo algorithm to discrete character specificity belong when host oak todifferent specificity when oak accompanied in by changes visuallytransitions from inspecttropical temperate whether to regionsvice and Additionally, we variation observed in This index
Acceptede Article also -
correlation within species (if individuals within aspecies ways),correlation species within and behave (if within insimilar individuals for a analysis). similar ad libitum
here used Gaussian MCMCglmms to used MCMCglmms to Gaussian is equivalent to Pagel’s
is individual larva, twosources ofnon is individual ) wer used phylogenetic reconstructions throughused phylogenetic reconstructions character mapping stochastic to states for extant species, extant for states
sample theposterior of statesof probability ancestral distribution host a e excluded from analysis. this e excluded
given trait s belong toasingle Singletons and rare 3larvae (i.e. species those withless than . Usingcomplete weevilphylogeny the
the phylogenetic As our w prediction
is explained byphylogeneticis explained among distance species λ
and
ranges from 0(nophylogeneticrangesfrom signal)( to1 infested investigate stochastic characterstochastic mapping - Quercus Quercus Quercus Quercus relatives breadth as thata relationshipas between
by each species. weevil - independence may data arise: ofthe 1) Finally, inlarval differences
the relationship betweenthe relationship thewidth of of their oak . Todeal clustered this with sections genus
section ). G Quercus the models (seethe models host iven a p iven (Appendix (Appendix
(Revell 2012) (Revell
vs s
( low phylogeneticlow i.e highi.e phylogenet applies aMonteapplies Since ourlevel of hylogeny andhylogeny genus sections (Huelsenbecket al. S larval - 1, versa were Sol etal.Sol
. Figure structure
head andhead all for ) .
the S 1) ic , This article isprotected rights by All copyright. reserved. 1). of specialization (Fig. host A2 inAppendix 3,Table The andtraitHost specialization relationships species replacement ( 0.05; in Weevil communities Nicaraguahigher a also ±0.03 diversity showed beta (0.78 diversity species richness Nicaragua held a Although independent ofthelineages phylogenetic ofthe thatmost Nicaraguan tree species showed well formeda more weevil California while inNicaraguatheesti consideredas species putative new GMYC groupsfromany Nicaragua published sequence, were matched hence tentatively they to assign to all larvae either grouped 14species into The final 778 Species andd delimitation R were withR performed including wi head
Accepted ArticleESULTS Quercus mean ofS index index
the number of oak species the number of
- species species Curculio Curculio cox1 ( ørensen index
χ ( χ higher higher dth as a responsedth asa variable and ²
² sequences California obtained, 529from andNicaragua, 249from were = = ha β 12.1 16 tu d trophic websremarkable showed differences regions terms between in - (R Core Team(R 2015) ) analysis. clustersGMYC afterlevel the alpha diversity yet and (Fig.1 be Table to discovered 1). consensus The .
9 from site to site (Fig. 2, Appendix from (Fig.Appendix tosite site 2, , p iversity patterns , p
of temperate weevils (Appendix of temperate weevils(Appendix Curculio occidentisCurculio
< 0.001
< ± standard deviation
0. 000 . S ) and in pecies accumulation curve pecies accumulation mated regional pool ofspeciesregional pool that mated suggests 1) Nicaragua , of
weevil
Simpson Simpson
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since
range ofoak in species -
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promote species coexistencepromote by species (Dyeret al.2007,Foriste Gibson (1977)
found n at the regionalor level, , (Lewinsohn and Roslin 2008) Roslin and (Lewinsohn associated withagreater showed that
in extrapolations basedextrapolations onHill )
the same oak hosts hosts oak the same in Nicaragua, which , found an outstandingfound
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This article isprotected rights by All copyright. reserved. Acceptedwereassociated acorns i inNicaragua not with larger but of therelationship Additional empirical con presentacorn their diets in broader species have differences performance inlarval innon the larvae(out ofa from ofthe 249) host emerged acornsof‘non equally both wellfrom inacorns potential hosts species labile trait (Nosil 2002) Articlebeen Previous work possibility towards hostspecializationinthe transition from atemperatedistribution toatropical be along position expected by theirthephylogeny. relative This Nicaraguan considered study inthis (Kergoat etal. andDelobel 2005,Delobel 2006) insects some tend toshow degreeconservatism ofphylogenetic reducing niche overlap y
developed smaller smaller developed common within lineagescommon within ofphytophagous insects
showed ashowed lower phylogenetic specificity, adistance higher i.e. phylogenetic among
among the supported by phylogenetic charactersupported with mapping by reconstructions stochastic evidence in support of the host specialization hypothesievidence ofthe specialization host insupport species species . acquired firmation Consistent with this suggestion this with Consistent points out points (Barrett Heil 2012) and between larval and ofthe size acorn body size species. host exhibited higherexhibited
weevils consideredweevils in more biochemical pathways tocope biochemical pathways ofcompoundsmore withthe variety . (Hutchinson 1959,Salisburyet(Hutchinson al.2012,Brown 201
. However, even. head
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host host , and thelarvae - wheneffects controlling for phylogenetic preferred host acor host preferred specialization specialization between generalization and specialization genus sections. genus sections. our ,
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This article isprotected rights by All copyright. reserved. original version a into wider form Acceptedhypothesis considerable hasreceived support mountain pa the relative stability environmental species’thermal tolerances could reduced making have al. 2012) pattern can be more thanone congeners the Nicaragua, particularly the by additional factors The larvalwider performance set ona ofhostspecies generalist Articleefficiency of host todifferencespoints in 2011) supported bycurrent evidence variation phenotypic plasticity grown bibliography (e.g. results are considering remarkable thatthe a tighter associated matching geographic
contrasting eco specialization , the existence of latitudinal , theexistence oflatitudinal ad libitum . in - . Fifty yearsFifty ago feeding scenario feeding scenario
Instead, t
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the result of population isolation followed ofpopulation isolation the result byallopatric speciation state distribution distribution
were thus included, Hughes &Hughes Vogler, 2004b) might - (Gibson 1969) (Gibson and he evolutionary scenarios . besides competition besides
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result in Daniel strikingly high of these tropical weevils might larval size with
(Desouhant et al. 2000, Hughes2004b,Bonalet and al.2000, Vogler etal.(Desouhant ion Janzen Janzen
promote biochemical
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species turnoverspecies component morphological related to biotic interactions tobiotic related
suggested bysuggested analyses also ourbeaffected may he s
but directly measured andbut directly measured
(Ghalambor et al.,2006) (Ghalambor in the rel ) high
formulated theformulated hypothesis thatinthe tropics -
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This article isprotected rights by All copyright. reserved. temperateregions Acceptedspecialization, biodiversitylatitudinal pattern but also biodiversity. patterns of diversification relationships among patterns provide system, with generationfactors ofmore andspecific the mechanisms into provide important insight Foristeral. et(2015 to improve statistical powergeneral and conclusions draw Certain ArticleA drawback oursisthe lack ofstudieslike 2002) specialized onthesame local adaptation habitats that so represent tropical montane restricted tolowlands montane ecosystems higher ratesinthetropics diversification .
ly, excellent from in the future
strong dispersal barriers.strong dispersal globaland multiple This research its its that of the restricteddispersal weevil remarkable remarkable to the availab ,
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and should beshould developed only not populations andspecies mismatchbetweenlatitudinal andplant insect ies host , which - le hosts, - . Robledo etRobledo al.,2016) clades ofthe tests
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Increasing ourknowledge of to insect a focusradiations regions and onparticular specific may still ,
could bethe by continue exploring
and diversity of acornand diversity of weevils study of how biotic and abiotic howfactors toshapestudycombine biotic of In addition, their oak arealso hosts tomontane restricted defies theory current ,
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hypotheses by less tolerant high to thanthose temperatures information along information
allow an host specialization host - the analysis of the acorn product of parallel evolution . Therefore, from the point ofview. Therefore,from of a the point , necessary ing the origin of .
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This article isprotected rights by All copyright. reserved. Blüthgen, N., Baselga,L. Orme. A.,and D.2012.Betapart:AnRpackage C. for diversity. thestudyof beta M.Ole andBascompte, Jordano, J. P. J., Barrett,L. 2012.UnifyingHeil. andmechanisms G.,and concepts inthespecificity M. of I.andAljanabi, 1997.Universal M.,and rapid S. Martinez. salt L project AGL2014 Atracción Talento de IBERO Synergy project post Ferran thephylogenetic with Sayol were helpful very analyses. partlya was supported G.P by provided valuablecomments an on draft initial (UNAN/Leonand M Belén Sánchez Urrutia, thankJosué We Bladimir Acuña (UNAN/Managua), A such an extraordinary uponwhichhost they depend, ITERATURE ITERATURE Accepted ArticleCKNOWLEDGEMENTS - metrics tell us about specialization and Ecologymetrics biologicalus about tell specialization traits? 89:3387 Methods inEcology 3:808 Evolution and FacilitateBiodiversity Maintenance. Science 312:431 plant genomicDNA doctor - REDD+ network funded by CYTED. network REDD+ – enemy interactions.Trends Science17:282 Plant in al
grantthe RamonAreces F from J. Fründ, D. P. Vázquez,anddo interaction Fründ, P. 2008.What F. network D. Menzel. J. - C Humanes
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, and Indiana, and Coronado – 433. the European Research Council
Keith Gaddis (UCLA)Keith Gaddis – - 292. extraction of highextraction quality
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This article isprotected rights by All copyright. reserved. Forister,L.,L.Novotny, M. L.Baje, V. Y. T.Butterill, A.K. Basset, P. Panorska, P. Cizek, T.Lill,L.Dyer, O.Stireman,L. G. J. Marquis, E. R. Gentry, Singer, A.,M.S. J. R.J. D thetropics.Dobzhansky, in American T.1950.Evolution 38:209 Scientist Desouh Delobel, inEuropeanand B., 2006.Dietary A.Delobel. groups species seed specialization of Brown, 2008.Seed constrainsgrowthBonal, growth of suppression seed and the R., A. Munoz. M.Espelta. Ortego, 2012.Positive cascade J. J. Bonal, and A.Muñoz, M. Hernández, R., selection M.Espelta, onlifeBonal, andComplex A.P.Vogler. J. 2011. R.,
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Supporting information – Appendix S1
Peguero G., Bonal R., Sol D., Muñoz A., Sork, V.L. & Espelta J.M.
Tropical insect diversity: evidence of greater host specialization in seed-feeding weevils. Ecology. 2017.
Table S1. Geographical coordinates, oak hosts, weevil species and number of larvae determined from each sampling site. Weevil species are molecularly delimited entities designated with preliminary numbers in Nicaragua (see main text for further details).
Region Locality nº Latitude Longitude Quercus species Curculio species Sample size [local name] 2 36º 3' 36"N 119º 2' 2"W lobata pardus 16 5 36º 28' 33"N 119º 7' 15"W lobata pardus 20 8 36º 43' 30"N 119º 27' 32"W lobata pardus; occidentis 17
10 37º 27' 43"N 119º 52' 48"W lobata; douglasii; wislizenii pardus; occidentis;aurivestis 19
11 37º 58' 44"N 120º 23' 16"W lobata; kellogii pardus; occidentis 18 14 38º 59' 45"N 121º 6' 28"W lobata; kellogii; wislizenii pardus; occidentis 31 15 39º 13' 37"N 121º 25' 19"W douglasii pardus 16 17 39º 42' 39"N 122º 0' 14"W lobata occidentis 2 27 39º 5' 10"N 122º 20' 45"W lobata; douglasii pardus 19 28 38º 44' 53"N 122º 37' 4"W lobata pardus; occidentis 15
31 37º 51' 54"N 122º 2' 2"W lobata occidentis 18
46 34º 24' 43"N 118º 34' 12"W lobata; agrifolia pardus 18 47 34º 11' 13"N 118º 53' 24"W lobata; agrifolia pardus; occidentis 19 68 39º 2' 35"N 122º 46' 30"W lobata; douglasii pardus; occidentis 20 California 71 38º 29' 35"N 122º 8' 52"W douglasii; wislizenii; berberidifolia pardus; occidentis 33 81 36º 50' 2"N 121º 33' 7"W lobata; kellogii; agrifolia occidentis; aurivestis 33 84 36º 5' 56"N 121º 9' 3"W agrifolia pardus; occidentis 11 86 36º 23' 6"N 121º 33' 28"W douglasii; agrifolia pardus; occidentis; aurivestis 29 91 34º 41' 56"N 120º 2' 24"W lobata; agrifolia; douglasii pardus; occidentis 34 97 37º 21' 14"N 121º 44' 27"W lobata; douglasii; agrifolia pardus; occidentis; aurivestis 28 112 34º 27' 18"N 119º 13' 48"W lobata; agrifolia pardus; occidentis 6 204 38º 59' 6"N 122º 58' 12"W douglasii; berberidifolia pardus; occidentis; aurivestis 25 207 38º 29' 10"N 120º 50' 45"W lobata pardus; occidentis 19 210 39º 38' 10"N 121º 56' 45"W lobata pardus; occidentis; aurivestis 13 211 33º 16' 19"N 117º 10' 58"W berberidifolia; engelmanii pardus 10 212 33º 16' 30"N 116º 37' 22"W agrifolia; engelmanii; cornelius-mullerii pardus; occidentis; aurivestis 9 213 33º 14' 6"N 117º 1' 19"W berberidifolia; engelmanii pardus 10 214 33º 3' 54"N 116º 24' 3"W engelmanii; cornelius-mullerii pardus; aurivestis 3 215 33º 2' 31"N 116º 19' 30"W engelmanii occidentis 1 1.Jalapa-Cruz 13° 55' 10"N 86° 8' 30"W sapotifolia; segoviensis #1, #7, #9, #14 21 2.Jalapa-Limón 13°53'15"N 86°12'31"W sapotifolia; segoviensis #7, #9, #14 11 3.Palacagüina 13°31'19"N 86°22'5"W segoviensis #1, #4, #9, #28 8
4.La Anona 13º30'5"N 86°22'12"W segoviensis #1, #4 8
5. Telpaneca 13°30'44"N 86°13'12"W segoviensis #1, #4, #9 6 6.Susukayán 13°36'1"N 86°10'15"W segoviensis #1, #9 6 7.Somoto 13°22'36"N 86°37'8"W segoviensis #1, #4, #11 13 Nicaragua 8.Las Sabanas 13°20'18"N 86°37'0"W insignis; segoviensis #1, #4, #11 27 9.El Robledal 13°12'44"N 86°17'36"W segoviensis #1, #4 26 10.Plan Helado 13°13'10"N 86°15'3"W segoviensis #1, #4, #11 28 11.El Zacatón 13°13'35"N 86°14'14"W cortesii; insignis #4, #12, #14, #40 10 12.Miraflor 13°14'21"N 86°13'24"W insignis #9, #12, #35 15 13.San Rafael 13°10'21"N 86°04'19"W segoviensis #1, #4, #7, #9, #11 16 14.Jinotega 13°03'47"N 85°59'29"W segoviensis #4, #12 4 15.Tisey 12°57'9"N 86°20'47"W segoviensis; sapotifolia #1, #4, #6, #7, #11, #14, #28 18 16. La Garnacha 12°59'1"N 86°21'58"W Elliptica #6, #14 16 17.Tomabú 13°00'59"N 86°17'31"W Segoviensis #1, #4, #11 16
Table S2. Curculio/Quercus interaction matrix in California (a) and Nicaragua (b). Weevil species are molecularly delimited entities designated with preliminary numbers in Nicaragua (see text for further details). Singletones and rare trophic interactions (i.e. supported with < 3 individuals) are shown but not included in herbivore richness counts (Novotny et al. 2012). Herbivore richness describes the number of Curculio species per host species. Interaction strength (%) is the number of emergences from the main host relative to all emergences. Specificity section level (%) reflects the number of emergences from the hosts of the same genus section relative to all emergences.
(a) California
Curculio/Quercus Erythrobalanus section Lepidobalanus section Σ Host Range Interaction Specificity section species strength (%) level (%) wislizenii kellogii agrifolia lobata douglasii berberidifolia Engelmanii cornelius-mulleri Occidentis 18 10 63 141 31 20 2 0 285 7 49.6 70 Aurivestis 0 0 2 9 10 0 1 3 25 5 40 92 Pardus 3 6 21 105 51 15 16 2 219 8 48.6 86.1 Σ individuals 21 16 86 255 92 35 19 5 529 - - - Herbivore richness 2 2 2 3 3 2 1 2 ------(b) Nicaragua
Curculio/Quercus species Erythrobalanus section Lepidobalanus section Σ individuals Host Interaction Specificity elliptica sapotifolia cortesii segoviensis insignis Range strength (%) section level (%) #1 0 0 0 68 1 69 2 98.6 100 #4 0 0 1 59 19 79 3 74.7 98.7 #6 12 1 0 0 0 13 2 92.3 100 #7 0 16 0 1 0 17 2 94.1 94.1 #9 0 0 0 22 1 23 2 95.7 100 #11 0 0 0 11 0 11 1 100 100 #12 0 0 0 1 14 15 2 93.3 100 #14 4 7 6 0 0 17 3 41.2 100 #28 0 1 0 1 0 2 2 50 50 #35 0 0 0 0 2 2 1 100 100 #40 0 0 1 0 0 1 1 100 100 Σ individuals 16 25 8 163 37 249 - - - Herbivore richness 2 2 1 4 2 ------Figure S1. Phylogeny of 29 acorn weevils (Curculio sp.) based in two mtDNA genes (cox1 and citB) and one nuclear gene (EF1α). Major rule consensus topology was inferred using Maximum Likelihood and Bayesian inference with a GTR+I+G substitution model. Bayesian probability value for node support is shown. Neotropical-Nicaraguan clades are highlighted in light blue whereas Nearctic and Palearctic clades are in orange and dark blue respectively.
Figure S2. Evolutionary transitions between tropical (blue color) and temperate (red) regions (left panel) and degree of host specialization (single Quercus genus section, red vs. >1 Quercus genus section, blue; right panel) of acorn weevils, Curculio genus. Historical trait distributions were reconstructed through stochastic character mapping (see text for details and references). Pie charts at nodes show the proportion of character values after 1000 simulations. According to the reconstructions, the Neotropics were colonized at least two times by temperate weevil ancestors, and this was associated with a trend to infest acorns of oak hosts belonging to a single genus section.
Table S3. Relationship between the width of weevil larval head and acorn volume in Nicaragua and California. Models are generalized linear mixed models based on Markov Chain Monte Carlo including phylogeny and species identity as random factors (see text for details and references). Abbreviations are as follows: post.mean = posterior mean, l-95% CI = lower limit of the 95% credible interval, u-95% CI = upper limit of the 95% credible interval, eff.sample= effective size of the sample, pMCMC=posterior probability for the parameter not being different from zero.
Model: head ~ log(acorn), random=~phylogeny+species
Nicaragua Effects eff.sample post.mean l-95% CI u-95% CI pMCMC Random Phylogeny 1000 0.0153 0.0003 0.0518 - Species 822 0.0059 0.0002 0.0204 - Residual 741 0.0177 0.0134 0.0228 - Fixed intercept 1000 0.6047 0.2224 0.9141 <0.001*** log(acorn) 1000 0.1061 0.0649 0.1429 <0.001*** Deviance Information Criterion = -134.13 Phylogenetic heritability = 0.38
California Effects eff.sample post.mean l-95% CI u-95% CI pMCMC Random Phylogeny 1000 0.8041 0.0002 0.5435 - Species 1000 0.1541 0.0002 0.1715 - Residual 1000 0.0101 0.0067 0.0137 - Fixed intercept 1000 1.0303 0.3765 1.9869 0.048* log(acorn) 939 0.0390 -0.0073 0.0945 0.116 Deviance Information Criterion = -100.63 Phylogenetic heritability = 0.83
LITERATURE CITED
Novotny, V., S. E. Miller, J. Hrcek, L. Baje, Y. Basset, O. T. Lewis, A. J. a Stewart, and G. D. Weiblen. 2012. Insects on plants: explaining the paradox of low diversity within specialist herbivore guilds. The American Naturalist 179:351–362.