Pelage variation and morphometrics of closely related Callithrix marmoset species and their hybrids.
Anthropogenic
Anthropogenic hybridization
Brazil
Dysgenesis
Heterosis
Hybridization
Transgressive segregation
Journal
BMC ecology and evolution
ISSN: 2730-7182
Titre abrégé: BMC Ecol Evol
Pays: England
ID NLM: 101775613
Informations de publication
Date de publication:
20 Sep 2024
20 Sep 2024
Historique:
received:
07
01
2024
accepted:
29
08
2024
medline:
21
9
2024
pubmed:
21
9
2024
entrez:
20
9
2024
Statut:
epublish
Résumé
Hybrids are expected to show greater phenotypic variation than their parental species, yet how hybrid phenotype expression varies with genetic distances in closely-related parental species remains surprisingly understudied. Here, we investigate pelage and morphometric trait variation in anthropogenic hybrids between four species of Brazilian Callithrix marmosets, a relatively recent primate radiation. Marmoset species are distinguishable by pelage phenotype and morphological specializations for eating tree exudates. In this work, we (1) describe qualitative phenotypic pelage differences between parental species and hybrids; (2) test whether significant quantitative differences exist between parental and hybrid morphometric phenotypes; and (3) determine which hybrid morphometic traits show heterosis, dysgenesis, trangression, or intermediacy relative to the parental trait. We investigated cranial and post-cranial morphometric traits, as most hybrid morphological studies focus on the former instead of the latter. Finally, we estimate mitogenomic distances between marmoset species from previously published data. Marmoset hybrid facial and overall body pelage variation reflected novel combinations of coloration and patterns present in parental species. In morphometric traits, C. jacchus and C. penicillata were the most similar, while C. aurita was the most distinct, and C. geoffroyi trait measures fell between these species. Only three traits in C. jacchus x C. penicillata hybrids showed heterosis. We observed heterosis and dysgenesis in several traits of C. penicillata x C. geoffroyi hybrids. Transgressive segregation was observed in hybrids of C. aurita and the other species. These hybrids were also C. aurita-like for a number of traits, including body length. Genetic distance was closest between C. jacchus and C. penicillata and farthest between C. aurita and the other species. We attributed significant morphometric differences between marmoset species to variable levels of morphological specialization for exudivory in these species. Our results suggest that intermediate or parental species-like hybrid traits relative to the parental trait values are more likely in crosses between species with relatively lesser genetic distance. More extreme phenotypic variation is more likely in parental species with greater genetic distance, with transgressive traits appearing in hybrids of the most genetically distant parental species. We further suggest that fewer developmental disturbances can be expected in hybrids of more recently diverged parental species, and that future studies of hybrid phenotypic variation should investigate selective pressures on Callithrix cranial and post-cranial morphological traits.
Sections du résumé
BACKGROUND
BACKGROUND
Hybrids are expected to show greater phenotypic variation than their parental species, yet how hybrid phenotype expression varies with genetic distances in closely-related parental species remains surprisingly understudied. Here, we investigate pelage and morphometric trait variation in anthropogenic hybrids between four species of Brazilian Callithrix marmosets, a relatively recent primate radiation. Marmoset species are distinguishable by pelage phenotype and morphological specializations for eating tree exudates. In this work, we (1) describe qualitative phenotypic pelage differences between parental species and hybrids; (2) test whether significant quantitative differences exist between parental and hybrid morphometric phenotypes; and (3) determine which hybrid morphometic traits show heterosis, dysgenesis, trangression, or intermediacy relative to the parental trait. We investigated cranial and post-cranial morphometric traits, as most hybrid morphological studies focus on the former instead of the latter. Finally, we estimate mitogenomic distances between marmoset species from previously published data.
RESULTS
RESULTS
Marmoset hybrid facial and overall body pelage variation reflected novel combinations of coloration and patterns present in parental species. In morphometric traits, C. jacchus and C. penicillata were the most similar, while C. aurita was the most distinct, and C. geoffroyi trait measures fell between these species. Only three traits in C. jacchus x C. penicillata hybrids showed heterosis. We observed heterosis and dysgenesis in several traits of C. penicillata x C. geoffroyi hybrids. Transgressive segregation was observed in hybrids of C. aurita and the other species. These hybrids were also C. aurita-like for a number of traits, including body length. Genetic distance was closest between C. jacchus and C. penicillata and farthest between C. aurita and the other species.
CONCLUSION
CONCLUSIONS
We attributed significant morphometric differences between marmoset species to variable levels of morphological specialization for exudivory in these species. Our results suggest that intermediate or parental species-like hybrid traits relative to the parental trait values are more likely in crosses between species with relatively lesser genetic distance. More extreme phenotypic variation is more likely in parental species with greater genetic distance, with transgressive traits appearing in hybrids of the most genetically distant parental species. We further suggest that fewer developmental disturbances can be expected in hybrids of more recently diverged parental species, and that future studies of hybrid phenotypic variation should investigate selective pressures on Callithrix cranial and post-cranial morphological traits.
Identifiants
pubmed: 39304843
doi: 10.1186/s12862-024-02305-3
pii: 10.1186/s12862-024-02305-3
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
122Subventions
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
ID : 302044/2014
Organisme : European Commission
ID : AMD-793641
Informations de copyright
© 2024. The Author(s).
Références
Mallet J. Hybridization as an invasion of the genome. Trends Ecol Evol. 2005;20(5):229–37. https://doi.org/10.1016/j.tree.2005.02.010 .
doi: 10.1016/j.tree.2005.02.010
pubmed: 16701374
Crispo E, Moore JS, Lee-Yaw JA, Gray SM, Haller BC. Broken barriers: Human-induced changes to gene flow and introgression in animals. BioEssays. 2011;33(7):508–18. https://doi.org/10.1002/bies.201000154 .
doi: 10.1002/bies.201000154
pubmed: 21523794
Grabenstein KC, Taylor SA. Breaking barriers: causes, consequences, and experimental utility of human-mediated hybridization. Trends Ecol Evol. 2018;33(3):198–212. https://doi.org/10.1016/j.tree.2017.12.008 .
doi: 10.1016/j.tree.2017.12.008
pubmed: 29306562
McFarlane SE, Pemberton JM. Detecting the true extent of introgression during anthropogenic hybridization. Trends Ecol Evol. 2019;34(4):315–26. https://doi.org/10.1016/j.tree.2018.12.013 .
doi: 10.1016/j.tree.2018.12.013
pubmed: 30655011
Adavoudi R, Pilot M. Consequences of hybridization in mammals: A systematic review. Genes. 2021;13(1):50. https://doi.org/10.3390/genes13010050 .
doi: 10.3390/genes13010050
pubmed: 35052393
pmcid: 8774782
Ottenburghs J. The genic view of hybridization in the Anthropocene. Evol Appl. 2021. https://doi.org/10.1111/eva.13223 .
doi: 10.1111/eva.13223
pubmed: 34745330
pmcid: 8549621
Moran BM, Payne C, Langdon Q, Powell DL, Brandvain Y, Schumer M. The genomic consequences of hybridization. eLife. 2021;10. https://doi.org/10.7554/elife.69016 .
Kirkpatrick M, Barton NH. Evolution of a Species’ Range. Am Nat. 1997;150(1):1–23. https://doi.org/10.1086/286054 . PMID: 18811273.
Burgarella C, Barnaud A, Kane NA, Jankowsky F, Scarcelli N, Billot C, et al. Adaptive introgression: an untapped evolutionary mechanism for crop adaptation. 2018. https://doi.org/10.1101/379966 .
doi: 10.1101/379966
Ackermann RR. Phenotypic traits of primate hybrids: Recognizing admixture in the fossil record. Evol Anthropol Issues News Rev. 2010;19(6):258–70. https://doi.org/10.1002/evan.20288 .
doi: 10.1002/evan.20288
Warren KA, Ritzman TB, Humphreys RA, Percival CJ, Hallgrímsson B, Ackermann RR. Craniomandibular form and body size variation of first generation mouse hybrids: A model for hominin hybridization. J Hum Evol. 2018;116:57–74. https://doi.org/10.1016/j.jhevol.2017.12.002 .
doi: 10.1016/j.jhevol.2017.12.002
pubmed: 29477182
pmcid: 6699179
Harvati K, Ackermann RR. Merging morphological and genetic evidence to assess hybridization in Western Eurasian late Pleistocene hominins. Nat Ecol Evol. 2022;6(10):1573–85. https://doi.org/10.1038/s41559-022-01875-z .
doi: 10.1038/s41559-022-01875-z
pubmed: 36064759
Kohn LAP, Langton LB, Cheverud JM. Subspecific genetic differences in the saddle-back tamarin (Saguinus fuscicollis) postcranial skeleton. Am J Primatol. 2001;54(1):41–56. https://doi.org/10.1002/ajp.1011 .
doi: 10.1002/ajp.1011
pubmed: 11329167
Bicca-Marques JC, Prates HM, de Aguiar FRC, Jones CB. Survey of Alouatta caraya, the black-and-gold howler monkey, and Alouatta guariba clamitans, the brown howler monkey, in a contact zone, State of Rio Grande do Sul, Brazil: evidence for hybridization. Primates. 2008;49(4):246–52. https://doi.org/10.1007/s10329-008-0091-4 .
doi: 10.1007/s10329-008-0091-4
pubmed: 18654738
Kelaita MA, Cortés-Ortiz L. Morphological variation of genetically confirmed Alouatta pigra×A. palliata hybrids from a natural hybrid zone in Tabasco, Mexico. Am J Phys Anthropol. 2012;150(2):223–234. https://doi.org/10.1002/ajpa.22196 .
Cogălniceanu D, Stănescu F, Arntzen JW. Testing the hybrid superiority hypothesis in crested and marbled newts. J Zool Syst Evol Res. 2019;58(1):275–83. https://doi.org/10.1111/jzs.12322 .
doi: 10.1111/jzs.12322
Nikolakis ZL, Schield DR, Westfall AK, Perry BW, Ivey KN, Orton RW, et al. Evidence that genomic incompatibilities and other multilocus processes impact hybrid fitness in a rattlesnake hybrid zone. Evolution. 2022. https://doi.org/10.1111/evo.14612 .
doi: 10.1111/evo.14612
pubmed: 36111705
Majtyka T, Borczyk B, Ogielska M, Stöck M. Morphometry of two cryptic tree frog species at their hybrid zone reveals neither intermediate nor transgressive morphotypes. Ecol Evol. 2022;12(1). https://doi.org/10.1002/ece3.8527 .
Boel C, Curnoe D, Hamada Y. Craniofacial shape and nonmetric trait variation in hybrids of the Japanese macaque (Macaca fuscata) and the Taiwanese macaque (Macaca cyclopis). Int J Primatol. 2019;40(2):214–43. https://doi.org/10.1007/s10764-019-00081-2 .
doi: 10.1007/s10764-019-00081-2
Stelkens RB, Schmid C, Selz O, Seehausen O. Phenotypic novelty in experimental hybrids is predicted by the genetic distance between species of cichlid fish. BMC Evol Biol. 2009;9(1):283. https://doi.org/10.1186/1471-2148-9-283 .
doi: 10.1186/1471-2148-9-283
pubmed: 19961584
pmcid: 2796671
Cheverud JM, Jacobs SC, Moore AJ. Genetic differences among subspecies of the saddle-back tamarin (Saguinus fuscicollis):evidence from hybrids. Am J Primatol. 1993;31(1):23–39. https://doi.org/10.1002/ajp.1350310104 .
doi: 10.1002/ajp.1350310104
pubmed: 32070080
Bell M, Travis M. Hybridization, transgressive segregation, genetic covariation, and adaptive radiation. Trends Ecol Evol. 2005;20(7):358–61. https://doi.org/10.1016/j.tree.2005.04.021 .
doi: 10.1016/j.tree.2005.04.021
pubmed: 16701394
Rieseberg LH, Archer MA, Wayne RK. Transgressive segregation, adaptation and speciation. Heredity. 1999;83(4):363–72. https://doi.org/10.1038/sj.hdy.6886170 .
doi: 10.1038/sj.hdy.6886170
pubmed: 10583537
Rieseberg LH, Widmer A, Arntz AM, Burke B. The genetic architecture necessary for transgressive segregation is common in both natural and domesticated populations. Philos Trans R Soc B Biol Sci. 2003;358(1434):1141–7. https://doi.org/10.1098/rstb.2003.1283 .
doi: 10.1098/rstb.2003.1283
Cortes-Ortiz L, Duda TF, Canales-Espinosa D, Garcia-Orduna F, Rodriguez-Luna E, Bermingham E. Hybridization in large-bodied New World primates. Genetics. 2007;176(4):2421–5. https://doi.org/10.1534/genetics.107.074278 .
doi: 10.1534/genetics.107.074278
pubmed: 17603105
pmcid: 1950642
Malukiewicz J, Cartwright RA, Curi NHA, Dergam JA, Igayara CS, Moreira SB, et al. Mitogenomic phylogeny of Callithrix with special focus on human transferred taxa. BMC Genomics. 2021;22(1). https://doi.org/10.1186/s12864-021-07533-1 .
Malukiewicz J, Boere V, de Oliveira MAB, D’arc M, Ferreira JVA, French J, et al. An introduction to the Callithrix genus and overview of recent advances in marmoset research. ILAR J. 2020;61(2–3):110–38. https://doi.org/10.1093/ilar/ilab027 .
doi: 10.1093/ilar/ilab027
pubmed: 34933341
Malukiewicz J. A review of experimental, natural, and anthropogenic hybridization in Callithrix marmosets. Int J Primatol. 2018;40(1):72–98. https://doi.org/10.1007/s10764-018-0068-0 .
doi: 10.1007/s10764-018-0068-0
Hershkovitz P. Comments on the taxonomy of Brazilian marmosets (Callithrix, Callitrichidae). Folia Primatol. 1975;24(2–3):137–72. https://doi.org/10.1159/000155687 .
doi: 10.1159/000155687
Hershkovitz P. Living New World monkeys (Platyrrhini). Chicago: University of Chicago Press; 1977.
Passamani M, Aguiar L, Machado R, Figueiredo E. Hybridization between Callithrix geoffroyi and Callithrix penicillata in southeastern Minas Gerais. Brazil Neotropical Primates. 1997;5:9–10.
doi: 10.62015/np.1997.v5.369
Mendes S. Padroes biogeograficos e vocais em Callithrix do grupo jacchus (Primates, Callitrichidae) ). PhD thesis, Dissertation. Universidade Estadual de Campinas (UNICAMP); 1997.
Ruiz-Miranda CR, Affonso AG, de Morais MM, Verona CE, Martins A, Beck BB. Behavioral and ecological interactions between reintroduced golden lion tamarins (Leontopithecus rosalia Linnaeus, 1766) and introduced marmosets (Callithrix spp, Linnaeus, 1758) in Brazil’s Atlantic Coast forest fragments. Braz Arch Biol Technol. 2006;49:99–109.
doi: 10.1590/S1516-89132006000100012
Malukiewicz J, Boere V, Fuzessy LF, Grativol AD, French JA, de Oliveira e Silva I, et al. Hybridization effects and genetic diversity of the common and black-tufted marmoset (Callithrix jacchus and Callithrix penicillata) mitochondrial control region. Am J Phys Anthropol. 2014;155(4):522–536. https://doi.org/10.1002/ajpa.22605 .
Fuzessy LF, de Oliveira Silva I, Malukiewicz J, Silva FFR, do Carmo Pônzio M, Boere V, et al. Morphological variation in wild marmosets (Callithrix penicillata and C. geoffroyi) and their hybrids. Evol Biol. 2014;41(3):480–493. https://doi.org/10.1007/s11692-014-9284-5 .
Cezar AM, Lopes GS, Cardim SS, Bueno C, Weksler M, Oliveira JA. Morphological and Genetic Variation Among Callithrix Hybrids in Rio de Janeiro. Brazil Evol Biol. 2023;50(3):365–80. https://doi.org/10.1007/s11692-023-09610-7 .
doi: 10.1007/s11692-023-09610-7
Yamamoto M. From dependence to sexual maturity: The behavioural ontogeny of Callitrichidae. In: Rylands A, editor. Marmosets and tamarins: Systematics, ecology and behaviour. Oxford: Oxford University Press; 1993. p. 235–54.
doi: 10.1093/oso/9780198540229.003.0011
Carvalho R. Conservação do saguis-da-serra-escuro (Callithrix aurita(Primates)) – Analise molecular e colormetrica de populações do gênero Callithrix e seus híbridos [dissertation]. Universidade do Estado do Rio de Janeiro; 2015.
Nagorsen DW, Peterson RL. Mammal collectors’ manual : a guide for collecting, documenting, and preparing mammal specimens for scientific research. Royal Ontario Museum; 1980.
R Core Team. R: A Language and Environment for Statistical Computing. Vienna; 2020. https://www.R-project.org/ .
Xie Y. Dynamic Documents with R and knitr. 2nd ed. Boca Raton: Chapman and Hall/CRC; 2015.
Wickham H, Vaughan D, Girlich M. tidyr: Tidy Messy Data. 2024. R package version 1.3.1. https://github.com/tidyverse/tidyr , https://tidyr.tidyverse.org . Accessed 01 Apr 2024.
Xie Y, Allaire J, Horner J. markdown: Render Markdown with ‘commonmark’. 2023. R package version 1.12. https://CRAN.R-project.org/package=markdown . Accessed 01 Apr 2024.
Wickham H, François R, Henry L, Müller K, Vaughan D. dplyr: A Grammar of Data Manipulation. 2023. R package version 1.1.4. https://github.com/tidyverse/dplyr , https://dplyr.tidyverse.org . Accessed 01 Apr 2024.
Wickham H. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York; 2016. https://ggplot2.tidyverse.org .
Wickham H. The Split-Apply-Combine Strategy for Data Analysis. J Stat Softw. 2011;40(1):1–29.
doi: 10.18637/jss.v040.i01
Fox J, Weisberg S. An R Companion to Applied Regression. 3rd ed. Thousand Oaks: Sage; 2019. https://socialsciences.mcmaster.ca/jfox/Books/Companion/ .
Kassambara A. rstatix: Pipe-friendly framework for basic statistical tests. 2021. R package version 0.7.0. https://CRAN.R-project.org/package=rstatix . Accessed 01 Apr 2024.
Kassambara A. ggpubr: ‘ggplot2’ Based Publication Ready Plots. 2023. R package version 0.6.0. https://CRAN.R-project.org/package=ggpubr . Accessed 01 Apr 2024.
Auguie B. gridExtra: Miscellaneous Functions for “Grid” Graphics. 2017. R package version 2.3. https://CRAN.R-project.org/package=gridExtra . Accessed 01 Apr 2024.
Läärä E. Statistics: Reasoning on uncertainty, and the insignificance of testing null. Ann Zool Fenn. 2009;46(2):138–57. https://doi.org/10.5735/086.046.0206 .
doi: 10.5735/086.046.0206
Araújo A, Arruda MF, Alencar AI, Albuquerque F, Nascimento MC, Yamamoto ME. Body Weight of Wild and Captive Common Marmosets (Callithrix jacchus. Int J Primatol. 2000;21(2):317–24. https://doi.org/10.1023/a:1005433722475 .
doi: 10.1023/a:1005433722475
Tamura K, Stecher G, Kumar S. MEGA11: Molecular evolutionary genetics analysis version 11. Mol Biol Evol. 2021;38(7):3022–7. https://doi.org/10.1093/molbev/msab120 .
doi: 10.1093/molbev/msab120
pubmed: 33892491
pmcid: 8233496
Stecher G, Tamura K, Kumar S. Molecular evolutionary genetics analysis (MEGA) for macOS. Mol Biol Evol. 2020;37(4):1237–9. https://doi.org/10.1093/molbev/msz312 .
doi: 10.1093/molbev/msz312
pubmed: 31904846
pmcid: 7086165
Caro T, Brockelsby K, Ferrari A, Koneru M, Ono K, Touche E, et al. The evolution of primate coloration revisited. Behav Ecol. 2021;32(4):555–67. https://doi.org/10.1093/beheco/arab029 . https://academic.oup.com/beheco/article-pdf/32/4/555/39805493/arab029.pdf
Santana SE, Lynch Alfaro J, Alfaro ME. Adaptive evolution of facial colour patterns in Neotropical primates. Proc R Soc B Biol Sci. 2012;279(1736):2204–11. https://doi.org/10.1098/rspb.2011.2326 . https://royalsocietypublishing.org/doi/pdf/10.1098/rspb.2011.2326
Winters S, Allen WL, Higham JP. The structure of species discrimination signals across a primate radiation. eLife. 2020;9:e47428. https://doi.org/10.7554/eLife.47428 .
Delhey K. A review of Gloger’s rule, an ecogeographical rule of colour: definitions, interpretations and evidence. Biol Rev. 2019;94(4):1294–316. https://doi.org/10.1111/brv.12503 . https://onlinelibrary.wiley.com/doi/abs/10.1111/brv.12503
Kamilar JM, Bradley BJ. Interspecific variation in primate coat colour supports Gloger’s rule. J Biogeogr. 2011;38(12):2270–2277. https://doi.org/10.1111/j.1365-2699.2011.02587.x . https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-2699.2011.02587.x . Accessed 10 Aug 2022.
Alvares CA, Stape JL, Sentelhas PC, de Moraes Gonçalves JL, Sparovek G. Köppen’s climate classification map for Brazil. Meteorol Z. 2013:711–728. Publisher: Schweizerbart’sche Verlagsbuchhandlung. https://doi.org/10.1127/0941-2948/2013/0507 . Accessed 10 Aug 2022.
Vital OV, Massardi NT, Brasileiro SLS, Côrrea TCV, Gjorup DF, Jerusalinsky L, et al. New Records for Callithrix aurita and Callithrix hybrids in the region of Viçosa, Minas Gerais. Brazil Neotropical Primates. 2020;26(2):104–9.
doi: 10.62015/np.2020.v26.59
Malukiewicz J, Cartwright RA, Dergam JA, Igayara CS, Kessler SE, Moreira SB, et al. The gut microbiome of exudivorous marmosets in the wild and captivity. Sci Rep. 2022;12(1). https://doi.org/10.1038/s41598-022-08797-7 .
Power ML, Oftedal OT. Differences among captive callitrichids in the digestive responses to dietary gum. Am J Primatol. 1996;40(2):131–44. https://doi.org/10.1002/(sici)1098-2345(1996)40:2<131::aid-ajp2>3.0.co;2-z .
doi: 10.1002/(sici)1098-2345(1996)40:2<131::aid-ajp2>3.0.co;2-z
Power ML, Myers EW. Digestion in the common marmoset (Callithrix jacchus), a gummivore-frugivore. Am J Primatol. 2009;71(12):957–63. https://doi.org/10.1002/ajp.20737 .
doi: 10.1002/ajp.20737
pubmed: 19725117
Caton JM, Hill DM, Hume ID, Crook GA. The digestive strategy of the common marmoset, Callithrix jacchus. Comp Biochem Physiol A Physiol. 1996;114(1):1–8. https://doi.org/10.1016/0300-9629(95)02013-6 .
doi: 10.1016/0300-9629(95)02013-6
pubmed: 8925425
de Souza VB. Variação do crânio e da mandíbula em Callithrix Erxleben, 1777 (Platyrrhini, Callitrichidae): resultados de uma abordagem através de morfometria geométrica. Universidade Federal de Viçosa; 2016.
Forsythe EC, Ford SM. Craniofacial adaptations to tree-gouging among marmosets. Anat Rec Adv Integr Anat Evol Biol. 2011;294(12):2131–9. https://doi.org/10.1002/ar.21500 .
doi: 10.1002/ar.21500
Eng CM, Ward SR, Vinyard CJ, Taylor AB. The morphology of the masticatory apparatus facilitates muscle force production at wide jaw gapes in tree-gouging common marmosets (Callithrix jacchus). J Exp Biol. 2009;212(24):4040–55. https://doi.org/10.1242/jeb.029983 .
doi: 10.1242/jeb.029983
pubmed: 19946083
pmcid: 4075048
Taylor AB, Vinyard CJ. Comparative analysis of masseter fiber architecture in tree-gouging (Callithrix jacchus) and nongouging (Saguinus oedipus) callitrichids. J Morphol. 2004;261(3):276–85. https://doi.org/10.1002/jmor.10249 .
doi: 10.1002/jmor.10249
pubmed: 15281057
Vinyard CJ, Wall CE, Williams SH, Mork AL, Armfield BA, de Oliveira Melo LC, et al. The evolutionary morphology of tree gouging in marmosets. In: The Smallest Anthropoids. Springer US; 2009. pp. 395–409. https://doi.org/10.1007/978-1-4419-0293-1_20 .
Pineda-Munoz S, Alroy J. Dietary characterization of terrestrial mammals. Proc R Soc B Biol Sci. 2014;281(1789):20141173. https://doi.org/10.1098/rspb.2014.1173 .
doi: 10.1098/rspb.2014.1173
CABANA F, DIERENFELD ES, Wirdateti, DONATI G, NEKARIS KAI. Exploiting a readily available but hard to digest resource: A review of exudativorous mammals identified thus far and how they cope in captivity. Integr Zool. 2018;13(1):94–111. https://doi.org/10.1111/1749-4877.12264 .
Nash LT. Dietary, behavioral, and morphological aspects of gummivory in primates. Am J Phys Anthropol. 1986;29(S7):113–37. https://doi.org/10.1002/ajpa.1330290505 .
doi: 10.1002/ajpa.1330290505
Smith AC. Exudativory in primates: interspecific patterns. In: The Evolution of Exudativory in Primates. Springer New York; 2010. pp. 45–87. https://doi.org/10.1007/978-1-4419-6661-2_3 .
Marroig G, Cropp S, Cheverud JM. Systematics and evolution of the jacchus group of marmosets (Platyrrhini). Am J Phys Anthropol. 2003;123(1):11–22. https://doi.org/10.1002/ajpa.10146 .
doi: 10.1002/ajpa.10146
Natori M, Shigehara N. Interspecific differences in lower dentition among eastern-Brazilian marmosets. J Mammal. 1992;73(3):668–71. https://doi.org/10.2307/1382041 .
doi: 10.2307/1382041
Natori M. Craniometrical variations among eastern Brazilian marmosets and their systematic relationships. Primates. 1994;35(2):167–76. https://doi.org/10.1007/bf02382052 .
doi: 10.1007/bf02382052
Rylands A, Faria D. In: Rylands A, editor. Habitats, feeding ecology, and home ranges size in the genus Callithrix. Press: Oxford University; 1993. p. 262–72.
Francisco TM, Couto DR, Zanuncio JC, Serrão JE, Silva IdO, Boere V. Vegetable Exudates as Food for Callithrix spp. (Callitrichidae): Exploratory Patterns. PLoS One. 2014;9(11):e112321. https://doi.org/10.1371/journal.pone.0112321 .
Bouchardet da Fonseca GA, Lacher TE. Exudate-feeding by Callithrix jacchus penicillata in semideciduous woodland (Cerradão) in central Brazil. Primates. 1984;25(4):441–449. https://doi.org/10.1007/bf02381667 .
Lamoglia JM, Boere V, Picoli EAdT, de Oliveira JA, Silva Neto CdMe, Silva IdO. Tree Species and Morphology of Holes Caused by Black-Tufted Marmosets to Obtain Exudates: Some Implications for the Exudativory. Animals. 2022;12(19):2578. https://doi.org/10.3390/ani12192578 .
Pinheiro HLN, Mendes Pontes AR. Home Range, Diet, and Activity Patterns of Common Marmosets (Callithrix jacchus) in Very Small and Isolated Fragments of the Atlantic Forest of Northeastern Brazil. Int J Ecol. 2015;2015:1–13. https://doi.org/10.1155/2015/685816 .
doi: 10.1155/2015/685816
Porter LM, Garber PA, Nacimento E. Exudates as a fallback food for Callimico goeldii. Am J Primatol. 2008;71(2):120–9. https://doi.org/10.1002/ajp.20630 .
doi: 10.1002/ajp.20630
Cezar AM, Pessoa LM, Bonvicino CR. Morphological and genetic diversity in Callithrix hybrids in an anthropogenic area in southeastern Brazil (Primates: Cebidae: Callitrichinae). Zoologia. 2017;34:1–9. https://doi.org/10.3897/zoologia.34.e14881 .
doi: 10.3897/zoologia.34.e14881
Malukiewicz J, Cartwright RA, Dergam JA, Igayara CS, Nicola PA, Pereira LMC, et al. Genomic skimming and nanopore sequencing uncover cryptic hybridization in one of world’s most threatened primates. Sci Rep. 2021;11(1):17279. https://doi.org/10.1038/s41598-021-96404-6 . Nature Publishing Group.