Santos, J.C., M. Baquero, C. Barrio-Amorós, L.A. Coloma, L.K. Erdtmann, A.P. Lima and D.C. Cannatella. 2104. Aposematism increases acoustic diversification and speciation in poison frogs. Proceedings of the Royal Society 281: 1-9.

Santos, J.C., M. Baquero, C. Barrio-Amorós, L.A. Coloma, L.K. Erdtmann, A.P. Lima and D.C. Cannatella. 2104. Aposematism increases acoustic diversification and speciation in poison frogs. Proceedings of the Royal Society 281: 1-9.

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  , 20141761, published 15 October 2014 281 2014 Proc. R. Soc. B    Albertina P. Lima and David C. CannatellaJuan C. Santos, Margarita Baquero, César Barrio-Amorós, Luis A. Coloma, Luciana K. Erdtmann,   speciation in poison frogsAposematism increases acoustic diversification and   Supplementary data tml "Data Supplement" References  This article cites 39 articles, 9 of which can be accessed free Subject collections  (201 articles)taxonomy and systematics (1919 articles)evolution (1240 articles)behaviour  Articles on similar topics can be found in the following collections Email alerting service   here right-hand corner of the article or click Receive free email alerts when new articles cite this article - sign up in the box at the top go to: Proc. R. Soc. B  To subscribe to on October 16, 2014rspb.royalsocietypublishing.orgDownloaded from on October 16, 2014rspb.royalsocietypublishing.orgDownloaded from Research Cite this article:  Santos JC, Baquero M,Barrio-Amoro´s C, Coloma LA, Erdtmann LK,Lima AP, Cannatella DC. 2014 Aposematismincreases acoustic diversification and speciationin poison frogs.  Proc. R. Soc. B  281 : 20141761. 15 July 2014Accepted: 17 September 2014 Subject Areas: behaviour, evolution, taxonomyand systematics Keywords: mating signals, aposematism, natural selection,sexual selection Author for correspondence: Juan C. Santose-mail:;infraguttatus@gmail.comElectronic supplementary material is availableat orvia Aposematism increases acousticdiversification and speciation inpoison frogs Juan C. Santos 1,2 , Margarita Baquero 3 , Ce´sar Barrio-Amoro´s 4 , Luis A. Coloma 5 ,Luciana K. Erdtmann 6 , Albertina P. Lima 6 and David C. Cannatella 7 1 Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4 2 National Evolutionary Synthesis Center, Suite A200, 2024 West Main St., Durham, NC 27705, USA 3 Department of Biological Sciences, Mississippi State University, Starkville, MS 39762, USA 4 Instituto de Biodiversidad Tropical, Uvita, Costa Rica 5 Centro Jambatu de Investigacio´n y Conservacio´n de Anfibios, Fundacio´n Otonga, Geovanni Farina 566 y Baltra,San Rafael, Quito, Ecuador 6 Instituto Nacional de Pesquisas da Amazoˆnia - INPA, Manaus, Amazonas, Brazil 7 Department of Integrative Biology and Texas Natural History Collections, University of Texas, 1 UniversityStation C0990, Austin, TX 78712, USA Multimodal signals facilitate communication with conspecifics during court-ship, but they can also alert eavesdropper predators. Hence, signallers facetwo pressures: enticing partners to mate and avoiding detection by enemies.Undefended organisms with limited escape abilities are expected to mini-mize predator recognition over mate attraction by limiting or modifyingtheir signalling. Alternatively, organisms with anti-predator mechanismssuch as aposematism (i.e. unprofitability signalled by warning cues) mightelaborate mating signals as a consequence of reduced predation. We hypoth-esize that calls diversified in association with aposematism. To test this, weassembled a large acoustic signal database for a diurnal lineage of apose-matic and cryptic/non-defended taxa, the poison frogs. First, we showedthat aposematic and non-aposematic species share similar extinction rates,and aposematic lineages diversify more and rarely revert to the non-aposematic phenotype. We then characterized mating calls based onmorphological (spectral), behavioural/physiological (temporal) andenvironmental traits. Of these, only spectral and temporal features wereassociated with aposematism. We propose that with the evolution of anti-predator defences, reduced predation facilitated the diversification of vocalsignals, which then became elaborated or showy via sexual selection. 1. Introduction Acoustic signals of courting males are often conspicuous to eavesdropping ene-mies, and these males face a trade-off between attracting partners and avoidingpredators [1]. Diurnal signallers are especially vulnerable to predation owing totheir increased visual and acoustic detectability [2]. These individuals mayavoid predation with a spectrum of strategies from crypsis to aposematism(the linking of a warning signal with a defensive strategy) [3]. Non-defendedindividuals usually signal from concealed places and rely on crypsis to avoiddetection. If predation pressure is strong, individuals may reduce the numberof signals, alter their schedule or switch communication channels [4]. By con-trast, aposematic individuals (aposemes) broadcast warning signals that may be detected by predators [5]. Consequently, the evolution of aposematism,with the resulting reduction in predation risk, may enhance the diversificationof mating signals and signallers. We tested this hypothesis by a phylogeneticanalysis of the vocalizations of aposematic and cryptic species of the poisonfrog family Dendrobatidae.Aposematism is a complex phenotype that links conspicuous signals withdefence (e.g. alkaloids). The association of these traits with other ecological & 2014 The Author(s) Published by the Royal Society. All rights reserved.  on October 16, 2014rspb.royalsocietypublishing.orgDownloaded from   adaptations, including metabolic and diet specializations,characterizes the aposematic syndrome in dendrobatids [6].Visual cues such as chromatic conspicuousness are often awarning signal to predators such as avian predators onpoison frogs [7]. By contrast, acoustic cues warn predatorssuchasbats,whichavoidtheultrasoundchirpsfromdefended,nocturnalmoths[8].Althoughboth visualandacousticsignalsmay alert predators, their combined effects might increase theeffectiveness of anti-predator defences [9].Somepredatorslocatetheirpreybyexploitingcomponentsof the prey’s signal. The efficacy of visual warning signalsdependsonlightconditionsandbackground[5].Conspicuousprey might be effectively cryptic if the incident light is too low[10]. By contrast, sound-oriented predators and parasitesrecognize long-range signals such as mating calls and whenin proximity switch to visual or chemical identification [4].For example,  Corethrella  midges locate male frogs by theircalls and then switch to olfaction or other senses to locate thenostrils of the male, from which they obtain a blood meal[11]. Natural selection should favour individuals that avoidpredator attacks by maximizing aposematic conspicuousness.Twogeneraltypesofmechanismsmayexplaintheoriginof aposematism: first, predator-related mechanisms, includingprey aggregation, dietary conservatism of predators and neo-phobia [5] and second, traits shaped primarily by naturalselection, which can then be co-opted as sexual ornamentsthrough sexual selection [12]. Aposemes might be better atattracting mates if predators associate their mating signalswith unprofitability and thus avoid courting individuals.Thus, under reduced predator pressure, aposemes mayevolvemoreeasilydetectedmatingsignalsviasexualselection.Poison frogs are a model clade for studies of the preda-tor–prey ecology of aposematism, which evolved at leastfour times in this group (figure 1). However, not all dendro- batids fit the stereotype of the brightly coloured, charismaticfrog. Most are cryptically coloured and rely on camouflage.By contrast, the aposematic species are visually conspicuousand defended by skin alkaloids [13] that are distasteful andat times toxic to predators (e.g. birds, crabs and snakes). Den-drobatids are mostly diurnal and use visual and acousticsignals for intraspecific communication [14]. Their vocaliza-tions are innate and highly stereotyped, but have easilyquantifiable variation among species. Within some species,females prefer males with greater calling performance [15,16]. Calling has a significant metabolic cost for male frogs [17]and aposematic dendrobatids have higher metabolic rates [6], but the relationship between acoustic signalling, aposematismand metabolic rates has not been explored in dendrobatids.Using phylogenetic methods, we tested whether acousticmating signals diversified in association with the multiplesrcins of aposematism. Our results support this postulateand provide evidence that aposematism is associated withincreased speciation rate in dendrobatids. We propose thatthe srcin of aposematism, with the resulting reduction inpredation risk, enabled mating calls of defended species todiversify via sexual selection. 2. Material and methods (a) Acoustic data and perching behaviour We collected 16657 advertisement calls from 172 species. Allrecordings were obtained from field collections and museumarchives (electronic supplementary material, Dataset S1). Thecalls are characterized by single pulses with little frequencymodulation (figure 1; electronic supplementary material, S1and Dataset S1). Field recordings were digitized with a samplingrate of 16 bits at a rate of 22 or 44 kHz and filtered for back-ground noise using a bandpass filter of 1–5 kHz. Spectrogramsand power spectra were estimated using a Fast Fourier Trans-form (FFT) analysis using a Blackman window, 900 samples of overlap among subsequent FFTs, and 3 dB filter bandwidth of 87.5 Hz. Homology of acoustic units was assessed following aphysiological definition in which the call is the sound unit pro-duced by a cycle of trunk muscle contraction resulting in anexpiratory event [18]. We used note-pulses, which have uniformtemporal, spectral and taxon-specific features, as the homologousacoustic units. Temporal features and spectral properties weremeasured from oscillograms, spectrograms and power spectra(electronic supplementary material, figure S2 and Text). Allacoustic variables were measured using R AVEN P RO  v. 1.4 [19].We analysed 18 call variables measured from note-pulses (hom-ologous acoustic units) as well as temperature recorded at thecalling site and body size (electronic supplementary material,figure S2 and table S1). For each call variable, the mean of theindividuals was used for analysis. Finally, we also qualitativelydescribed perch (calling) site as exposed or concealed based onpublished and direct observations for 83 species (electronicsupplementary material, Dataset S1). (b) Alkaloid sequestration and conspicuousnessvariables We compiled skin alkaloid information of 97 taxa (electronic sup-plementary material, table S1). Species were characterized bytheir ability to sequester alkaloids as state 1 (able to sequester)or 0 (unable to sequester) [6]. A species was characterized asaposematic by the presence of defensive dietary alkaloids [6]and visual conspicuousness (electronic supplementary material,tables S1 and S2).Chromatic contrast against a natural background is con-sidered a measurement of conspicuousness to predators [6].Few dendrobatids have been assessed for conspicuousnessusing direct approaches such as total reflectance flux andmodels of predator perception [3,7]. Quantifying conspicuous- ness in life for 172 taxa using direct techniques was intractable.Therefore, we measured relative conspicuousness based onhuman perception of colour contrast against a leaf litter back-ground. Some authors [20] validly criticize the quantification of colouration based on human perception. These criticisms donot necessarily invalidate our analyses because most receiversinclude a mixture of trichromatic conspecifics and di-, tri- andtetrachromatic predators (electronic supplementary material, S1for discussion). All these receivers also have visual sensitivitiesthat overlap with the human vision range (400–700 nm) andmay not obtain information from the UV range [21].As a proxy for direct approaches, we formulated a binaryassessment of conspicuousness against a leaf litter background(electronic supplementary material, figure S3 and table S2).Colour descriptions of live male specimens were quantified bymultiple independent human observers (  X  ¼ 2 : 8 + 1 : 17 s : d : per species; electronic supplementary material, table S2).Using 11 frog skin segments, chromatic contrast (i.e. differentfrom grey, brown and black) was scored as 1 (conspicuous) or0 (cryptic). The total contrast score (TCS or  S S i ), whichranged from 0 (no contrast) to 11 (maximum contrast), wasdetermined by summing all 12 binary values. To account forinter-observer variation, we used six cut-off values ( S S i  3, S S i  4,  . . . , S S i  8; electronic supplementary material, figureS3) of increasing colour contrast thresholds. These thresholdsranged from liberal (a species with S S i  3 (TCS3) is categorized r     s      p   b     .r     o     y   a  l        s    o   c   i        e   t        y     p   u   b    l       i        s   h    i       n     g   . o  r       g   P    r    o   c    .R     . S      o   c    . B     2    8   1     :    2     0    1    4    1    7     6    1     2  on October 16, 2014rspb.royalsocietypublishing.orgDownloaded from    body mass and mass-corrected metabolic rates were transformedusing natural logarithms to improve statistical distributionproperties for the comparative procedures [22]. (d) Phylogenetic and comparative analyses The phylogeny was inferred from new and published moleculardata: approximately 2400 bp 12S–16S rDNA mitochondrialgenes (electronic supplementary material, table S1 for GenBanknumbers). The statistics of the molecular data matrix were asfollows: (i) total sequence length ( N  ¼ 172,   X  ¼ 2330 : 13 + 293 : 54 bp, missing cells are 13910/414692 or 3.35%);(ii) total sequence length per rRNA gene (12S:  N  ¼ 172,  X  ¼ 903 : 84 + 105 : 89 bp, missing cells are 3.44%; 16S:  N  ¼ 172,  X  ¼ 1358 : 88 + 175 : 42 bp, missing cells are 4.03%); and (iii) totalsequence length per tRNA gene ( t Val :  N  ¼ 172,   X  ¼ 67 : 41 + 12 : 89 bp, missing cells are 7.65%). Tree estimation and nodalsupport were calculated under maximum-likelihood (ML) andBayesian approaches using partitioned models. ML and BayesiananalysesgavesimilartreetopologiesandtheMLtreewasusedasastarting tree topology for the time-calibrated tree (electronic sup-plementary material, S1). The chronogram (figure 1; electronicsupplementary material, S1) was determined using BEASTv. 1.5.3 [23] with five node-age constraints (electronic supplemen-tary material, figure S1). Based on these analyses, two taxonomicchanges are made:  Ameerega erythromos  and  Colostethus jacobuspe-tersi  as part of   Hyloxalus  (i.e.  H. erythromos  and  H. jacobuspetersi ;new combinations; see electronic supplementary material, S1 fordetails). Chronogram tree file is deposited in the TreeBASEdatabase under the accession number 16380.To quantify the relationship between components of apose-matism and call variables, we used diversification analyses,multivariate data exploration, tests of phylogenetic signal andmodels of trait evolution, bivariate phylogenetic correlations,exploratory factor analyses (phylogenetic principal componentanalysis, PPCA) and phylogenetic logistic regressions (PLRs).Using the binary variables alkaloid sequestration and conspicu-ousness, we estimated the rates of speciation ( l 0  and  l 1 ),extinction ( m 0  and  m 1 ) and transition between character states( q 01  and  q 10 ) using Binary State Speciation and Extinction(BiSSE) models [24]. Multivariate data explorations and variablereduction were used to narrow the dataset to 18 variables (169taxa) that loaded on three principal components.The PLRs were used to determine if call variables significantlypredicted alkaloid sequestration and conspicuousness as depen-dent binary variables. Our predictors were two sets of continuousvariables: the three PCs (principal components) derived from thePPCA of the call characters, and individual call variables, with body size and temperature as covariates. PLRs were performedwith the PLogReg routine [25], which tests for phylogenetic signalwhile simultaneously performing the regressions. We applied thepercentage increase in odds and the ‘divide-by-4 rule’ (i.e.  b  /4where  b   is the regression coefficient) to determine significance of logistic regression coefficients [26]. See electronic supplementarymaterial, S1 for an example of   b  /4 interpretation. Outliers wereidentified using standardized residuals with absolute values morethan 3.0 and Cook’s distance more than 1.0 as criteria. For pairwisecorrelations between the discrete dependent variables, we usedPagel’s1994testforcorrelationoftwobinarycharacters[27].Signifi-cance of all analyses was determined at  a ¼ 0.05, two-taileddistribution. 3. Results We tested if acoustic courtship cues are associated with thesrcin of the aposematic phenotype, and if these patternsare related to species diversification. Specifically, (i) wedetermined whether conspicuousness and alkaloid sequestra-tion, the components of aposematism, are correlated andshow phylogenetic signal; (ii) we measured species diversifi-cation by comparing extinction, speciation and character-statetransition rates between aposematic and cryptic species;(iii) we used PPCA to describe the relationship betweencall variables and each aposematic component; and (iv) weused PLR to determine which call variables are associatedwith aposematism.In analysis (i), we used Pagel’s l [27] to test for phylogeneticsignal ( l . 0) in each of the two aposematic components scored(electronicsupplementarymaterial,figureS4andtableS3).Alka-loid sequestration showed phylogenetic signal ( p , 0.001),as did conspicuousness variables TCS3–TCS6 (all  p , 0.001).Alkaloid-bearingspeciesweremostlyconspicuous(allTCSvari-ables; all correlations significant at  p  0.032). Thus, aposematicspecies tend to be closely related and not randomly distributedacross the phylogeny.In analysis (ii), we used BiSSE models [24] to estimaterates of speciation ( l ), extinction ( m ) and transition betweenalternative character states ( q ). Given the concern about theinterpretation of BiSSE models with less than 300 terminals[28], we assessed statistical power (electronic supplementarymaterial, S1). As determined by simulations, our sample size(172 terminals) was adequate for analyses of speciation andtransition rates, but less so for extinction rates.The speciation rate for conspicuous lineages showed a1.36- to 2.18-fold increase over that in cryptic lineages,except for TCS6 ( p , 0.05 for all; figure 2; electronic sup-plementary material, S4). However, for alkaloid-bearinglineages neither the speciation rate nor the extinction ratewas different from that of non-defended lineages ( p . 0.05for all). Given that the speciation rate for conspicuouslineages was higher, it is surprising that defended cladesdid not have a high speciation rate, because conspicuousnessand sequestration are generally highly correlated. This resultis perhaps explainable by the large amount of missing datafor alkaloid sequestration (figure 1). However, it does notalter the general conclusion that aposematic clades have ahigher speciation rate. The extinction rate for conspicuouslineages was not different from that for cryptic lineages( p . 0.05 for all) except for TCS3.We found that the rate of change from inability (state 0) toability (state 1) to sequester alkaloids is 14 times higher thanthe reverse ( q 01 ¼ 0.014 versus  q 10 , 0.001;  p ¼ 0.044; figure 2;electronic supplementary material, S4); essentially no rever-sals from the defended to the non-defended phenotypehave taken place. Similarly, the transition rate from crypticto conspicuous states ( q 01 ) and the reverse ( q 10 ) shifted froma higher rate ( q 01 . q 10  in TCS3 and TCS5; all  p  0.011)to a lower rate ( q 01 , q 10  in variables TCS7 and TCS8; all p  0.007). This is supported by two more pieces of evidence:TCS5 was significantly correlated with alkaloid sequestra-tion ( p , 0.001), and TCS5 was also the best predictor of aposematism based only on conspicuousness (electronic sup-plementary material, figure S4). However, these resultssuggest that conclusions about rates of state change dependon how the binary state is defined, such as when large tip-ratios (more than 10:1) exist for change between states [28].In summary, the extinction rates of aposematic and crypticclades are not distinguishable, but aposematic lineagesspeciate more and are unlikely to revert to the cryptic/non-defended phenotype. r     s      p   b     .r     o     y   a  l        s    o   c   i        e   t        y     p   u   b    l       i        s   h    i       n     g   . o  r       g   P    r    o   c    .R     . S      o   c    . B     2    8   1     :    2     0    1    4    1    7     6    1     4  on October 16, 2014rspb.royalsocietypublishing.orgDownloaded from 
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