Our reference: YANBE 20191 P-authorquery-v1 AUTHOR QUERY FORM Journal: YANBE Article Number: 20191 Dear Author, During the preparation of your manuscript for typesetting, some questions have arisen. These are listed below. Please check your typeset proof carefully and mark any corrections in the margin of the proof or compile them as a separate list*. Bibliography If discrepancies were noted between the literature list and the text references, the following may apply: The references listed below were noted in the text but appear to be missing from your literature list. Please complete the , list or remove the references from the text. Uncited references: This section comprises references that occur in the reference list but not in the body of the text. , Please position each reference in the text or delete it. Any reference not dealt with will be retained in this section. Queries and/or remarks Location in Query / remark Response article Q1 One or more sponsor names may have been edited to a standard format that enables better searching and identification of your article. Please check and correct if necessary: 1) National Science Foundation, U.S.A. Q2 Please update Ref. ‘Drea, 2014’. Q3 Please check the journal title in Ref. ‘Simons and Rumpler, 1988’. Q4 Please confirm that given names and surnames have been identified correctly. Please check this box or indicate your approval if you have no , corrections to make to the PDF file Thank you for your assistance. *In case artwork needs revision, please consult http://authors.elsevier.com/artwork YANBE20191_grabs ■ 5 August 2014 ■ 1/1 Animal Behaviour xxx (2014) 1 5 Contents lists available at ScienceDirect 6 7 Animal Behaviour 8 9 10 journal homepage: www.elsevier.com/locate/anbehav 11 12 13 14 15 1 16 2 17 3 Highlights 4 Chemical profiles differ substantially between species across strepsirrhines. Urine markers express more urinary compounds than do nonurine markers. Signal richness is linked to various aspects of the focal species' socioecology. Chemical signals evolve gradually and at fast rates in strepsirrhines. http://dx.doi.org/10.1016/j.anbehav.2014.07.009 0003-3472/© 2014 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. Please cite this article in press as: delBarco-Trillo, J., & Drea, C. M., Socioecological and phylogenetic patterns in the chemical signals of strepsirrhine primates, Animal Behaviour (2014), http://dx.doi.org/10.1016/j.anbehav.2014.07.009 YANBE20191_proof ■ 5 August 2014 ■ 1/5 Animal Behaviour xxx (2014) 1e5 55 Contents lists available at ScienceDirect 56 57 Animal Behaviour 58 59 60 journal homepage: www.elsevier.com/locate/anbehav 61 62 63 Special Issue: Biochemistry & Animal Communication 64 65 1 Socioecological and phylogenetic patterns in the chemical signals of 66 2 67 3 strepsirrhine primates 68 4 69 a, * b, c 5 Q4 Javier delBarco-Trillo , Christine M. Drea 70 6 a 71 7 Museo Nacional de Ciencias Naturales, CSIC, Madrid, Spain b Department of Evolutionary Anthropology, Duke University, Durham, NC, U.S.A. 72 8 c Department of Biology, Duke University, Durham, NC, U.S.A. 73 9 74 10 75 11 article info 76 12 Our understanding of chemical signals in mammals derives principally from studies in which researchers 77 13 Article history: examine signal structure or function within a single species. Despite the unique information to be gained 78 14 Received 20 March 2014 from applying comparable methods across multiple species, comparative studies of chemical signals are 79 Initial acceptance 20 May 2014 extremely limited. Here, we review the available literature on the evolution of chemosignals in male and 15 80 Final acceptance 7 July 2014 female strepsirrhine primates (galagos, lorises and lemurs), all of which rely heavily on chemical 16 81 Available online xxx communication. We draw from a few case studies, but focus our review on two comparative studies. In 17 MS. number: 14-00226 one, researchers examined the volatile chemical composition of urinary signals across 12 species rep- 82 18 resenting most families within Strepsirrhini, including six ‘urine-marking’ species and six glandular or 83 19 Keywords: ‘nonurine-marking’ species. In the other, researchers examined the volatile chemical composition of 84 20 body odour glandular signals in eight Eulemur species differing in social or dominance structure. We highlight five 85 chemical signal 21 findings. (1) Regardless of the scent source, chemical profiles differ substantially between species, 86 22 comparative study ‘ ’ gas chromatography/mass spectrometry providing reliable species scent signatures . None the less, (2) urine markers express more compounds 87 23 olfactory communication and have more distinguishable species scent signatures in their urine than do nonurine markers, sug- 88 e 24 semiochemistry gesting specialization of function. Within Eulemur (3) chemical richness is greater in multimale mul- 89 tifemale species than in pair-bonded species. Moreover, (4) whereas chemical richness of male signals is 25 signal evolution 90 26 socioecology greater in sexually codominant species, chemical richness of female signals is greater in female- species difference fi 91 27 dominant species. Together, the ndings from both comparative studies, coupled with case studies, Strepsirrhini suggest that signal richness is linked to some aspect of the focal species' socioecology. Lastly, (5) 92 28 regardless of the scent source, strepsirrhine chemosignals evolve gradually over time, but at fast rates 93 29 and homogeneously within different lineages. Comparative studies reveal patterns that cannot be 94 30 detected from the single-species approach and are therefore critical for providing new insight into the 95 31 function and evolution of olfactory signals. 96 32 © 2014 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. 97 33 98 34 99 35 100 36 101 37 Chemical signals convey information about individuals and (Crawford, Boulet, & Drea, 2011; Greene & Drea, 2014; Hayes, 102 38 their physiological states (Wyatt, 2014). As in other mammals, Morelli, & Wright, 2006; Scordato et al., 2007), identity (Palagi & 103 39 intraspecific studies on the composition of primate chemical sig- Dapporto, 2006; Penn et al., 2007; Scordato et al., 2007; Smith, 104 40 nals (reviewed in e.g. Drea, 2014; Epple, 1986; Michael, Bonsall, & Tomlinson, Mlotkiewicz, & Abbott, 2001) and ‘quality’ (as esti- 105 41 Zumpe, 1976) have shown that these chemical signals can contain mated by genetic diversity: Boulet, Crawford, Charpentier, & Drea, 106 42 information about the signaller's sex (Belcher, Smith, Jurs, Lavine, & 2010; Charpentier, Boulet, & Drea, 2008; as estimated by major 107 43 Epple, 1986; Crewe, Burger, Roux, & Katsir, 1979; Greene & Drea, histocompatibility complex genotype: Setchell et al., 2011), as well 108 44 2014; Hayes, Morelli, & Wright, 2004; Penn et al., 2007; Scordato, as the genetic relatedness between individuals (Boulet, 109 45 Dubay, & Drea, 2007; Setchell et al., 2010), reproductive state Charpentier, & Drea, 2009; Charpentier et al., 2008; Morelli et al., 110 46 2013). 111 47 In contrast to the emphasis placed on intraspecific studies, 112 48 there have been exceptionally few mammalian studies in which 113 49 * Correspondence: J. delBarco-Trillo, Museo Nacional de Ciencias Naturales, researchers used a comparative approach to analyse chemical 114 50 Consejo Superior de Investigaciones Científicas (CSIC), Calle Jose Gutierrez Abascal data (Belcher et al., 1986; Decker, Ringelberg, & White, 1992; 115 51 2, 28006 Madrid, Spain. 116 E-mail address: [email protected] (J. delBarco-Trillo). Zabaras, Richardson, & Wyllie, 2005). Comparative studies can 52 117 53 http://dx.doi.org/10.1016/j.anbehav.2014.07.009 118 54 0003-3472/© 2014 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. 119 Please cite this article in press as: delBarco-Trillo, J., & Drea, C. M., Socioecological and phylogenetic patterns in the chemical signals of strepsirrhine primates, Animal Behaviour (2014), http://dx.doi.org/10.1016/j.anbehav.2014.07.009 YANBE20191_proof ■ 5 August 2014 ■ 2/5 2 J. delBarco-Trillo, C. M. Drea / Animal Behaviour xxx (2014) 1e5 1 be methodologically challenging (delBarco-Trillo, Burkert, COMPARATIVE STUDIES REVEAL ‘SPECIES SCENT SIGNATURES’ 66 2 Goodwin, & Drea, 2011; Drea et al., 2013), but can provide a 67 3 wealth of information about species differences relevant to un- In the first study to examine how the composition of chemical 68 4 derstanding broader socioecological patterns, as well as unique signals might differ between strepsirrhine species, Hayes et al. 69 5 insights into the evolution of chemical signals across different (2004) compared the volatile composition of secretions deriving 70 6 phylogenetic scales (Symonds & Elgar, 2008). Here, we review from the anogenital area in two phylogenetically distant species 71 7 recent comparative studies on the volatile composition of (L. catta and the Coquerel's sifaka, Propithecus coquereli). As antic- 72 8 chemical signals in strepsirrhine primates to elucidate whether ipated, the authors found that the chemical profiles of these two 73 9 socioecological factors correlate with the composition of chemical species' secretions were chemically distinct. Given that these spe- 74 10 signals and to uncover the mode and speed of chemical signal cies differ in their glandular structures (notably, the scrotal gland of 75 11 evolution. male L. catta is species specific; Montagna & Yun, 1962)