Abstract
Evolutionary theory and observation predict wider phenotypic variation in hybrids than parental species. Emergent phenotypic novelty in hybrids may in turn drive new adaptations or speciation by breaking parental phenotypic constraints. Primate hybridization is often documented through genetic evidence, but knowledge about the primate hybrid phenotype remains limited due to a small number of available studies on hybrid primate morphology. Here, we examine pelage and morphometric variation in two Brazilian marmoset species (Callithrix penicillata and C. geoffroyi) and their hybrids. Hybrids were sampled in an anthropogenic hybrid zone in the municipality of Viçosa, Minas Gerais state, Brazil. We analyzed hybrid facial and body pelage color variation, and compared 13 morphometric measures between hybrids and parental species. Five different hybrid facial morphotypes were observed, varying from intermediate to parental-like. Hybrid facial morphotypes were biased towards C. penicillata, suggesting that the pelage of this species may be dominant to that of C. geoffroyi in this context, and indicating that mate preference, and therefore gene flow/introgression, may be biased towards C. penicillata within the hybrid zone. Hybrid morphometric features were on average intermediate to parental species traits, but transgressive hybrids were also observed, suggesting that morphometric variation for the studied traits is consistent with Rieseberg’s complementary allele model. Finally, we observed a decoupling of facial patterning and size/shape in hybrids, relative to parent phenotypes, suggesting that an important factor driving phenotypic novelty within the Viçosa marmoset hybrid zone might be the loosening of evolutionary constraints on phenotypic trait integration.
Similar content being viewed by others
References
Ackermann, R. R. (2010). Phenotypic traits of primate hybrids: Recognizing admixture in the fossil record. Evolutionary Anthropology, 19, 258–270.
Ackermann, R. R., & Bishop, J. M. (2010). Morphological and molecular evidence reveals recent hybridization between gorilla taxa. Evolution, 64, 271–290.
Ackermann, R. R., Rogers, J., & Cheverud, J. M. (2006). Identifying the morphological signatures of hybridization in primate and human evolution. Journal of Human Evolution, 51, 632–645.
Affonso, A. G., Ruiz-Miranda, C. R., & Beck, B. (2004). Interações ecológicas entre mico leão dourado (Leontopithecus rosalia linnaeus,1766) reintroduzido e mico-estrela (Callithrix jacchus linnaeus,1758) introduzido em fragmentos de Mata Atlântica, R.J. A Primatologia no Brasil, 8, 123–134.
Allendorf, F., Leary, R., Spruell, P., & Wenburg, J. (2001). The problems with hybrids: Setting conservation guidelines. Trends in Ecology & Evolution, 16, 613–622.
Alonso, C., de Faria, D. S., Langguth, A., & Santee, D. F. (1987). Variação da pelagem na área de intergradação entre Callithrix jacchus e Callithrix penicillata. Revista Brasileira de Biologia, 47, 465–470.
Amaral, A. R., Lovewell, G., Coelho, M. M., Amato, G., & Rosenbaum, H. C. (2014). Hybrid speciation in a marine mammal: The Clymene dolphin (Stenellaclymene). PLoS ONE, 9, e83645.
Arnold, M. L. (2006). Evolution through genetic exchange. New York: Oxford University Press.
Arnold, M. L. (2008). Reticulate evolution and humans—Origins and ecology. New York: Oxford University Press.
Baack, E. J., & Rieseberg, L. H. (2007). A genomic view of introgression and hybrid speciation. Current Opinion in Genetics & Development, 17, 513–518.
Bell, M. A., & Travis, M. P. (2005). Hybridization, transgressive segregation, genetic covariation, and adaptive radiation. Trends in Ecology & Evolution, 20, 358–361.
Bicca-Marques, J. C., Prates, H. M., Aguiar, F. R. C., & Jones, C. B. (2008). 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, 49, 246–252.
Bonhomme, M., Cuartero, S., Blancher, A., & Crouau-roy, B. (2009). Assessing natural introgression in 2 biomedical model species, the rhesus macaque (Macaca mulatta) and the long-tailed macaque (Macaca fascicularis). Journal of Heredity, 100, 158–169.
Cavalcanti, G. C., & Langguth, A. (2008). Recognition of mate and speciation in marmoset genus Callithrix (Primates, Cebidae, Callithriquinae). Revista Nordestina de Biologia, 19, 59–73.
Cheverud, J. M., Jacobs, S. C., & Moore, A. J. (1993). Genetic differences among subspecies of the saddle-back tamarin (Saguinus fuscicollis): Evidence from hybrids. American Journal of Primatology, 31, 23–39.
Chiba, S. (2005). Appearance of morphological novelty in a hybrid zone between two species of land snail. Evolution, 59, 1712–1720.
Coimbra-Filho, A. F., Mittermeier, R. A., Rylands, A. B., Mendes, S. L., Kierulff, M. C. M., & Pinto, L. P. S. (2006). The taxonomic status of Wied’s black-tufted-ear marmoset, Callithrix kuhlii (Callitrichidae, Primates). Primate Conservation, 21, 1–24.
Cortés-Ortiz, L., Duda, T. F., Canales-Espinosa, D., García-Orduña, F., Rodriguez-Luna, E., & Bermingham, E. (2007). Hybridization in large-bodied New World primates. Genetics, 176, 2421–2425.
Czypionka, T., Cheng, J., Pozhitkov, A., & Nolte, A. W. (2012). Treanscriptome changes after genome wide admixture in invasive sculpins (Cottus). Molecular Ecology, 21, 4797–4810.
Detwiler, K. M., Burrell, A. S., & Jolly, C. J. (2005). Conservation implications of hybridization in African cercopthecine monkeys. International Journal of Primatology, 26, 661–684.
Digby, L. J., Ferrari, S. F., & Saltzman, W. (2007). Callitrichines: The role of competition in cooperatively breeding species. In C. J. Campbell, A. Fuentes, & K. C. MacKinnon (Eds.), Primates in perspective (pp. 85–106). New York: Oxford University Press.
Dittrich-Reed, D. R., & Fitzpatrick, B. M. (2013). Transgressive hybrids as hopeful monsters. Evolutionary Biology, 40, 310–315.
Epple, G., Belcher, A. M., Kuderling, I., Zeller, U., Scolnock, L., Greenfield, K. L., et al. (1993). Making sense out of scents: Species differences in scent glands, scent-marking behavior, and scent-mark composition in the Callitrichidae. In A. B. Rylands (Ed.), Marmosets and tamarins: Systematics, behaviour, and ecology (pp. 123–151). New York: Oxford University Press.
Falconer, D. S. (1981). Introduction of quantitative genetics. London: Longman Press.
Froelich, J. W., & Supriatna, J. (1996). Secondary intergradation between Macaca maurus and M. tonkeana in south Sulawesi, and the species status of M. togeanus. In J. Fa & D. Lindbergh (Eds.), Evolution and ecology of macaque societies (pp. 43–70). Cambridge: Cambridge University Press.
Hershkovitz, P. (1968). Metachromism: On the principle of evolutionary change in mammalian tegumentary colors. Evolution, 22, 556–575.
Hershkovitz, P. (1975). Comments on taxonomy of Brazilian marmosets (Callithrix, Callitrichidae). Folia Primatologica, 24, 137–172.
Hershkovitz, P. (1977). Living new world monkeys (Platyrrhini). Chicago: University of Chicago Press.
Kelaita, M. A., & Cortes-Ortiz, L. (2013). Morphological variation of genetically confirmed Alouatta pigra × A. palliate hybrids from a hybrid zone in Tabasco, Mexico. American Journal of Physical Anthropology, 150, 223–234.
Kohn, L. A. P., Langton, L. B., & Cheverud, J. M. (2001). Subspecific genetic differences in the saddle-back tamarin (Saguinus fusciocollis) postcranial skeleton. American Journal of Primatology, 54, 41–56.
Larsen, P. A., Marchan-Rivadeneira, M. R., & Baker, R. J. (2010). Natural hybridization generates mammalian lineage with species characteristics. PNAS, 107, 11447–11452.
Malukiewicz, J. (2013). Hybridization and speciation in common and black-tufted marmosets (Callithrix jacchus and C. penicillata). PhD Dissertation, Arizona State University, Tempe, Arizona.
Mendes, S. L. (1997a). Hybridization in free-ranging Callithrix flaviceps and the taxonomy of the Atlantic Forest marmosets. Neotropical Primates, 5, 6–8.
Mendes, S. L. (1997b). Padrões biogeográficos e vocais em Callithrix do grupo jacchus (Primates, Callithricidae). PhD Dissertation, Unversidade Estadual de Campinas, Campinas, São Paulo.
Nagel, U. (1973). Comparison of anubis baboons, hamadryas baboons and their hybrids at a species border in Ethiopia. Folia Primatologica, 19, 104–165.
Nagorsen, D. W., & Peterson, R. L. (1980). Mammal collectors manual. Toronto: The Royal Ontario Museum.
Parsons, K. J., Son, Y. H., & Albertson, R. C. (2011). Hybridization promotes evolvability in African cichlids: Connections between transgressive segregation and phenotypic integration. Evolutionary Biology, 38, 306–315.
Passamani, M., Aguiar, L. M. S., Machado, R. B., & Figueiredo, E. (1997). Hybridization between Callithrix geoffroyi and Callithrix penicillata in southeastern Minas Gerais, Brazil. Neotropical Primates, 5, 9–10.
Pereira, D. M. (2010). Densidade, genética e saúde populacional como ferramentas para propor um plano de controle e erradicação de invasão biológica: o caso de Callithrix aurita (Primates) no Parque Nacional da Serra dos Órgãos, RJ, Brasil. Universidade do Estado do Rio de Janeiro, Rio de Janeiro, RJ, Brazil.
Perelman, P., Johnson, W. E., Roos, C., Seuanez, H. N., Horvath, J. E., et al. (2011). A molecular phylogeny of living primates. PLoS Genetics, 7, e1001342.
Phillips-Conroy, J. E., & Jolly, C. J. (1981). Sexual dimorphism in two subspecies of Ethiopian baboons (Papio hamadryas) and their hybrids. American Journal of Physical Anthropology, 56, 115–129.
Pritchard, V. L., Knutson, V. L., Ziebra, M. L. J., & Edmands, S. (2012). Fitness and morphological outcomes of many generations of hybridization in the copepod Tigriopus californicus. Journal of Evolutionary Biology, 26, 416–433.
Renaud, S., Alibert, P., & Auffray, J. C. (2012). Modularity as a source of new morphological variation in the mandible of hybrid mice. BMC Evolutionary Biology, 12, 141.
Ribeiro, M. C., Metzger, J. P., Martensen, A. C., Ponzoni, F. J., & Hirota, M. M. (2009). The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation, 142, 1141–1153.
Rieseberg, L. H., Archer, M. A., & Wayne, R. K. (1999). Transgressive segregation, adaptation and speciation. Heredity, 83, 363–372.
Rieseberg, L. H., Widmer, A., Arntz, A. M., & Burke, J. M. (2003). The genetic architecture necessary for transgressive segregation is common in both natural and domesticated populations. Philosophical Transactions of the Royal Society of London. Series B, 358, 1141–1147.
Ruiz-Miranda, C., Affonso, A., de Morais, M., Verona, C., Martins, A., & Beck, B. (2006). 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. Brazilian Archives of Biology and Technology, 49, 99–109.
Ruiz-Miranda, C. R., Affonso, A. G., Martins, A., & Beck, B. (2000). Distribuição do sagüi (Callithrix jacchus) nas áreas de ocorrência do mico-leão-dourado (Leontopithecus rosalia) no Estado do Rio. Neotropical Primates, 8, 98–100.
Rylands, A. B., Coimbra-Filho, A. F., & Mittermeier, R. A. (1993). Systematics, distributions, and some notes on the conservation status of the Callitrichidae. In A. B. Rylands (Ed.), Marmosets and tamarins: Systematics, behaviour and ecology (pp. 11–77). Oxford: Oxford University Press.
Rylands, A. B., Coimbra-Filho, A. F., & Mittermeier, R. A. (2009). The systematics and distributions of the marmosets (Callithrix, Callibella, Cebuella, and Mico) and Callimico (Callimico) (Callitrichidae, primates). In S. M. Ford, L. M. Porter, & L. C. Davis (Eds.), The smallest anthropoids: The marmoset/callimico radiation (pp. 25–61). New York: Springer.
Rylands, A. B., Spironelo, W. R., Tornisielo, V. L., de Sá, R. L., Kierulff, M. C. M., & Santos, I. B. (1988). Primates of the Rio Jequitinhonha valley, Minas Gerais, Brazil. Primate Conservation, 9, 100–109.
Samuels, A., & Altmann, J. (1986). Immigration of a Papio anubis male into a group of Papio cynocephalus baboons and evidence for an anubis-cynocephalus hybrid zone in Amboseli, Kenya. International Journal of Primatology, 7, 131–138.
Santana, S. E., Lynch Alfaro, J., & Alfaro, M. E. (2012). Adaptive evolution of facial colour patterns in Neotropical primates. Proceedings of the Royal Society B: Biological Sciences, 279, 2204–2211.
Seehausen, O. (2004). Hybridization and adaptive radiation. Trends in Ecology & Evolution, 19(4), 198–207.
Tagliaro, C. H., Schneider, M. P., Schneider, H., Sampaio, I. C., & Stanhope, M. J. (1997). Marmoset phylogenetics, conservation perspectives, and evolution of the mtDNA control region. Molecular Biology and Evolution, 14, 674–684.
Tardif, S. D., Smucny, D. A., Abbott, D. H., Mansfield, K., Schultz-Darken, N., & Yamamoto, M. E. (2003). Reproduction in captive common marmosets (Callithrix jacchus). Comparative Medicine, 53, 364–368.
Templeton, A. R. (1987). Inferences on natural population structure from genetic studies of captive mammalian populations. In B. D. Chepko-Sade & Z. T. Halpin (Eds.), Mammalian dispersal patterns (pp. 257–272). Chicago: University of Chicago Press.
Vivo, M. (1991). Taxonomia de Callithrix Erxleben, 1777 (Callitrichidae, Primates). Belo Horizonte: Fundação Biodiversitas.
Yamamoto, M. E. (1993). From dependence to sexual maturity: The behavioural ontogeny of Callitrichidae. In A. B. Rylands (Ed.), Marmosets and tamarins: Systematics, ecology and behaviour (pp. 235–254). Oxford: Oxford University Press.
Zimmerman, D. W., & Zumbo, B. D. (2009). Hazards in choosing between pooled and separate-variances t tests. Psicologica, 30, 371–390.
Zinner, D., Groeneveld, L. F., Keller, C., & Roos, C. (2009). Mitochondrial phylogeography of baboons (Papio spp.)—Indication for introgressive hybridization? BMC Evolutionary Biology, 9, 83.
Acknowledgments
The authors would like to thank CAPES for providing a graduate scholarship to L.F.F. A Fulbright Fellowship and National Science Foundation Doctoral Dissertation Grant #1061508 to J.M. also provided additional funding for this work. We thank the Brasilia Zoo and Brasilia Botanical Garden for access to their premises.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Fuzessy, L.F., Silva, I.O., Malukiewicz, J. et al. Morphological Variation in Wild Marmosets (Callithrix penicillata and C. geoffroyi) and Their Hybrids. Evol Biol 41, 480–493 (2014). https://doi.org/10.1007/s11692-014-9284-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11692-014-9284-5