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Special Series of Articles - 60 Years of The Brazilian Society of Genetics • Genet. Mol. Biol. 39 (4) • Oct-Dec 2016 • https://doi.org/10.1590/1678-4685-GMB-2016-0091   copy

Molecular data highlight hybridization in squirrel monkeys (Saimiri, Cebidae)

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Hybridization has been reported increasingly frequently in recent years, fueling the debate on its role in the evolutionary history of species. Some studies have shown that hybridization is very common in captive New World primates, and hybrid offspring have phenotypes and physiological responses distinct from those of the "pure" parents, due to gene introgression. Here we used the TA15 Alu insertion to investigate hybridization in the genus Saimiri. Our results indicate the hybridization of Saimiri boliviensis peruviensis with S. sciureus macrodon, and S. b. boliviensis with S. ustus. Unexpectedly, some hybrids of both S. boliviensis peruviensis and S. b. boliviensis were homozygous for the absence of the insertion, which indicates that the hybrids were fertile.

Keywords
Saimiri; squirrel monkeys; Alu elements; hybridization

The Neotropical squirrel monkey genus Saimiri is one of the many platyrrhine taxa subject to controversy and uncertainty in terms of its species diversity and phylogenetic relationships (Alfaro et al., 2015Alfaro JWL, Boubli JP, Paim FP, Ribas CC, Da Silva MNF, Messias MR, Röhe F, Mercês MP, Júnior JSS and Silva CR (2015) Biogeography of squirrel monkeys (genus Saimiri): South-central Amazon origin and rapid pan-Amazonian diversification of a lowland primate. Mol Phylogenet Evol 82:436-454.). This genus is distributed primarily in the Amazon basin and Guianas (Figure 1), except Saimiri oerstedii, which is found in Central America, Costa Rica and Panama (Chiou et al., 2011Chiou KL, Pozzi L, Alfaro JWL and Di Fiori A (2011) Pleistocene diversification of living squirrel monkeys (Saimiri spp.) inferred from complete mitochondrial genome sequences. Mol Phylogenet Evol 59:736-745.). One of the most recent biogeographical studies of Saimiri (Alfaro et al., 2015Alfaro JWL, Boubli JP, Paim FP, Ribas CC, Da Silva MNF, Messias MR, Röhe F, Mercês MP, Júnior JSS and Silva CR (2015) Biogeography of squirrel monkeys (genus Saimiri): South-central Amazon origin and rapid pan-Amazonian diversification of a lowland primate. Mol Phylogenet Evol 82:436-454.) indicated that the species diversity of the genus is the product of a recent pan-Amazonian radiation. Based on the 14 clades identified in the analysis of the mitochondrial DNA (D-loop and cytb), these authors suggested a provisional taxonomy consisting of S. sciureus, S. oerstedii (S. o. oerstedii and S. o. citronellus), S. collinsi, S. ustus (A, B, and C lineages), S. boliviensis, S. cassiquiarensis (S. c. cassiquiarensis, S. c. albigena, S. c. macrodon A, S. c. macrodon B, and S. c. macrodon C), and S. vanzolinii. Analyzing mitochondrial DNA (CoxI and CoxII), Ruiz-García et al. (2015)Ruiz-García M, Luengas-Villamil K, Leguizamon N, De Thoisy B and Gálvez H (2015) Molecular phylogenetics and phylogeography of all the Saimiri taxa (Cebidae, Primates) inferred from mt COI and COII gene sequences. Primates 56:145-161. proposed the following classification: S. oerstedii, with two subspecies (S. o. oerstedii and S. o. citrinellus), S. vanzolinii and S. sciureus, with two subspecies, S. s. boliviensis [with two lineages: 1 (boliviensis) and 2 (peruviensis)] and S. s. sciureus [with 12 lineages: 1 (sciureus), 2(cassiquiarensis), 3(ustus I=A), 4(ustus II = B), 5(ustus III = C), 6 (macrodon I=D),7(macrodon II = E), 8 (macrodon III = F), 9 (macrodon IV = G), 10 (macrodon V = H), 11 (collinsi) and 12 (albigena)].

Figure 1
Map showing the geographical distributions of Saimiri species and the original sites where each one of the five populations studied was found. The majority of S. b. boliviensis specimens where captured in Santa Cruz de La Sierra, Bolivia (region in green) and later transported to CAPRIM in Argentina. Those from S. b. peruviensis (region in blue) and S. sciureus macrodon species (region in red) where captured in the vicinity of Iquitos, Peru, and then transported to CRCP/IVITA in Iquitos. S. ustus (region in orange) and S. collinsi specimens (region in aquamarine blue) were captured and sampled in the forest.

Saimiri populations occupy ample geographic areas (Figure 1), with many potential zones of contact that provide opportunities for hybridization between neighboring taxa (Hershkovitz, 1984Hershkovitz P (1984) Taxonomy of squirrel monkeys genus Saimiri (Cebidae, Platyrrhini): A preliminary report with description of a hitherto unnamed form. Am J Primatol 6:257-312.). Thorington Jr (1985)Thorington Jr RW (1985) The taxonomy and distribution of squirrel monkeys (Saimiri). In: Rosenblum LA and Coe CL (eds) Handbook of Squirrel Monkey Research. Springer, New York, pp 1-33. reported cases of hybridization between S. ustus and S. sciureus on the east bank of the Tapajós River. Silva et al. (1992)Silva BTF, Sampaio MIC, Schneider H, Schneider MPC, Montoya E, Encarnacion F and Salzano FM (1992) Natural hybridization between Saimiri taxa in the Peruvian Amazonia. Primates 33:107-113. investigated 49 specimens from a region in Peru occupied by both S. b. peruviensis and S. s. macrodon. By analyzing biochemical markers, these authors found clear evidence of admixture in approximately 45% of the individuals. Costello et al. (1993)Costello RK, Dickinson C, Rosenberger AL, Boinski S and Szalay FS (1993) Squirrel monkey (genus Saimiri) taxonomy. In: Kimble WH and Martin LB (eds) Species, Species Concepts and Primate Evolution. Springer, Boston, pp 177-210. also reported hybrids between S. ustus and S. sciureus from a region between the Madeira and Tapajós rivers.

Natural hybridization is the subject of a great deal of debate due to its potential importance as an evolutionary mechanism, especially for speciation, in addition to its relevance for taxonomy, conservation and species extinction (Mallet, 2005Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecology Evol 20:229-237., 2007Mallet J (2007) Hybrid speciation. Nature 446:279-283.; Genovart, 2009Genovart M (2009) Natural hybridization and conservation. Biodiv Conserv 18:1435-1439.;). Hybridization is known to have played a role in the evolutionary history of at least one quarter of plants and 10% of animal species (Rieseberg, 1997Rieseberg LH (1997) Hybrid origins of plant species. Annu Rev Ecol Syst 28:359-389.; Seehausen, 2004Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecology Evol 19:198-207.). Arnold and Meyer (2006)Arnold ML and Meyer A (2006) Natural hybridization in primates: One evolutionary mechanism. Zoology 109:261-276. concluded that reticulate evolution is a common process in the evolutionary history of animals, with numerous examples of the formation of new taxa as a consequence of introgressive hybridization. In primates, this phenomenon has been reported in both captivity and the natural environment (Schreiber et al., 1998Schreiber A, Wang M and Kaumanns W (1998) Captive breeding of squirrel monkeys, Saimiri sciureus and Saimiri boliviensis: the problem of hybrid groups. Zoo Biol 17:95-109.; Zinner et al., 2009Zinner D, Groeneveld LF, Keller C and Roos C (2009) Mitochondrial phylogeography of baboons (Papio spp.) - Indication for introgressive hybridization? BMC Evol Biol 9:e83.; Matauschek et al., 2011Matauschek C, Roos C and Heymann EW (2011) Mitochondrial phylogeny of tamarins (Saguinus, Hoffmannsegg 1807) with taxonomic and biogeographic implications for the S. nigricollis species groupAm J Phys Anthropol 144:564-574.). However, the exact role of hybridization in the evolutionary history of an organism is usually unclear, and reticulate evolution represents a potential pitfall for phylogenetic reconstructions. Arnold and Meyer (2006)Arnold ML and Meyer A (2006) Natural hybridization in primates: One evolutionary mechanism. Zoology 109:261-276. suggested that the accuracy of some phylogenetic constructs of New World monkeys is probably weakened by hybridization events that occurred in the past. While it is difficult to detect hybridization events, Osterholz et al. (2008)Osterholz M, Vermeer J, Walter L and Roos C (2008) A PCR-based marker to simply identify Saimiri sciureus and S. boliviensis boliviensis. Am J Primatol 70:1177-1180. described the integration of an Alu element in S. boliviensis, which is absent in S. sciureus.

In the human genome, Alu elements are the most abundant transposable features (Kriegs et al., 2007Kriegs JO, Churakov G, Jurka J, Brosius J and Schmitz J (2007) Evolutionary history of 7SL RNA-derived SINEs in Supraprimates. Trends Genet 23:158-161.), and these elements are now known to comprise approximately 10% of the primate genome (Batzer and Deininger, 2002Batzer MA and Deininger PL (2002) Alu repeats and human genomic diversity. Nat Rev Genet 3:370-379.; Zhang et al., 2002Zhang Z, Harrison P and Gerstein M (2002) Identification and analysis of over 2000 ribosomal protein pseudogenes in the human genome. Genome Res 12:1466-1482.). Once inserted into the genome of a species during its evolutionary history, Alu insertions will be present in all the descendants of that species. An Alu insertion is thus a single and irreversible event (Hamdi et al., 1999Hamdi H, Nishio H, Zielinski R and Dugaiczyk A (1999) Origin and phylogenetic distribution of Alu DNA repeats: irreversible events in the evolution of primates. J Mol Biol 289:861-871.; Shedlock and Okada, 2000Shedlock A and Okada N (2000) SINE insertions: Powerful tools for molecular systematic. Bioessays 22:148-160.; Salem et al., 2003Salem A-H, Ray DA, Xing J, Callinan PA, Myers JS, Hedges DJ, Garber RK, Witherspoon DJ, Jorde LB and Batzer MA (2003) Alu elements and hominid phylogenetics. Proc Natl Acad Sci U S A 100:12787-12791.), and represents a marker free of homoplasies. The present study investigated the potential occurrence of hybridization in free-living populations of S. boliviensis, based on the presence or absence of AluTA15, as described by Osterholz et al. (2008)Osterholz M, Vermeer J, Walter L and Roos C (2008) A PCR-based marker to simply identify Saimiri sciureus and S. boliviensis boliviensis. Am J Primatol 70:1177-1180..

We examined 107 samples of Saimiri: two S. sciureus macrodon, 16 S. collinsi, 17 S. ustus, 22 S. boliviensis peruviensis and 50 S. b. boliviensis (Table 1). All the individuals sampled were born in the wild, although in some cases, the blood samples were collected in captivity. The samples of S. collinsi were collected from animals captured during the rescue operation of the UHE Tucurui hydroelectric reservoir in Para, Brazil (La Rovere and Mendes, 2000La Rovere E and Mendes F (2000) Tucuruí Hydropower Complex, Brazil. A WCD Case Study Prepared as an Input to the World Commission on Dams. Cape Town World Commission on Dams Secretariat, Cape Town, 195 p.), and those of S. ustus at UHE Samuel, in Rondonia (Fearnside, 2005Fearnside MP (2005) Brazil's Samuel Dam: Essons for hydro-electric development policy and the environment in Amazonia. Environ Manag 35:1-19.). The samples of S. b. boliviensis, S. b. peruviensis and S. s. macrodon were obtained from two captive facilities, the "Centro de Reproducción y Conservación de Primates No Humanos" (CRCP/IVITA) in Iquitos, Peru, and the "Centro Argentinode Primates" (CAPRIM) in Corrientes, Argentina. The species were identified based on the morphological characteristics described by Hershkovitz (1984)Hershkovitz P (1984) Taxonomy of squirrel monkeys genus Saimiri (Cebidae, Platyrrhini): A preliminary report with description of a hitherto unnamed form. Am J Primatol 6:257-312.. S. b. boliviensis has a white zone around the eyes exhibiting sparse white hairs and a flattened arch over the eyes (roman arch) while in S. s macrodon the arch formed above each eye is more evident and has been named as a "gothic arch".

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Table 1
Species, specimen code, locality, geographical coordinates and origin of the specimens analyzed in the present study.

While S. b. boliviensis and S. b. peruviensis have an arch that is less pronounced over the eyes (roman arch), S. b. peruviensis has a crown pattern on the head which is less eumelanized than that of S. b. boliviensis. The specimens held at CRCP/IVITA were classified as S. boliviensis peruviensis (roman arch) and those from the vicinity of Iquitos (Figure 1) as S. sciureus macrodon (gothic arch), while the animals at CAPRIM, captured in Santa Cruz de La Sierra, Bolivia, were all S. boliviensis boliviensis (roman arch). Some of the animals at CAPRIM were born in captivity. Further details on the specimens and the geographical distribution of each population are presented in Table 1 and Figure 1. The material analyzed in the present study was part of the sample bank maintained by the Molecular Phylogenetics Laboratory at the Bragança campus of the Federal University of Para.

The total DNA was extracted using the Wizard Genomic kit (Promega, Madison, WI, USA) following the manufacturer's recommendations. The region of interest (AluTA15) was amplified using the primers and the protocol described by Osterholz et al. (2008)Osterholz M, Vermeer J, Walter L and Roos C (2008) A PCR-based marker to simply identify Saimiri sciureus and S. boliviensis boliviensis. Am J Primatol 70:1177-1180.. The initial denaturation step was 2 min at 94 °C, followed by 40 cycles of denaturation (1 min at 94 °C), annealing (1 min at 58 °C), and extension (1 min at 72 °C), with a final extension step of 5 min at 72 °C. After amplification, the PCR products were separated electrophoretically in a 2% agarose gel at 60 V, 150 mA for 60 min together with a 1 kb plus DNA ladder (Invitrogen, Carsbad, CA, USA). All the fragments were stained with GelRed, as recommended by the manufacturer (Biotium, Hayward, CA, USA). Sequence reactions were conducted with a Big Dye v.3.1 kit (ABI BigDye® Terminator Mix; Applied Biosystems, Carlsbad, CA, USA), conducted in an ABI 3500xL sequencer (Applied Biosystems), to confirm that the region amplified by PCR was the fragment of interest (AluTA15). The sequences were aligned and edited manually in the BioEdit program (Hall, 1999Hall TA (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95-98.).

The primers designed by Osterholz et al. (2008)Osterholz M, Vermeer J, Walter L and Roos C (2008) A PCR-based marker to simply identify Saimiri sciureus and S. boliviensis boliviensis. Am J Primatol 70:1177-1180. amplify fragments of distinct sizes depending on the presence or absence of the Alu insertion (AluTA15). When the AluTA15 insertion is present, a fragment of approximately 750 base pairs (bps) is generated, but when it is absent, a fragment of only 450 bps is generated. As the insertion is only present in S. boliviensis (Figure 2), in hybrids between this species and other Saimiri species, two fragments will be amplified, one with 750 bps and another with 450 bps.

Figure 2
Electrophoresis gel showing the distribution of the three Alu genotypes (+/+; +/-; and -/-) in the five subspecies sampled in the present study. A 1 kb ladder placed at both sides of the gel indicates the size in base pairs (bp) of the two amplified fragments.

The AluTA15 insertion was not detected in any of the individuals identified as S. ustus (n=17) from Rondonia, S. collinsi (n=16) from Para or S. sciureus macrodon (n=2) from Peru. All 35 individuals presented only one band of approximately 450 bps (Table 2). By contrast, 50 specimens from Santa Cruz de La Sierra, Bolivia, identified as S. b. boliviensis, presented the insertion, of which 90% were homozygous (+/+) and 10% (five individuals) were heterozygous (+/-) showing both bands (750 bps and 450 bps). This configuration was unexpected because Osterholz et al. (2008)Osterholz M, Vermeer J, Walter L and Roos C (2008) A PCR-based marker to simply identify Saimiri sciureus and S. boliviensis boliviensis. Am J Primatol 70:1177-1180. proposed that the AluTA15 element was inserted into the lineage that originated the extant species S. boliviensis, which implies that all S. boliviensis should be homozygous for AluTA15 (+/+). Interestingly, all three possible combinations were found in the population previously identified as S. b. peruviensis from Peru (CRCP), with six individuals (28%) being homozygous for the insertion (+/+), eight (36%) being homozygous for its absence (-/-), and the other eight being heterozygous (+/-), showing both bands (750/450 bps) in the gel (Figure 2). Osterholz et al. (2008)Osterholz M, Vermeer J, Walter L and Roos C (2008) A PCR-based marker to simply identify Saimiri sciureus and S. boliviensis boliviensis. Am J Primatol 70:1177-1180. also found three possible patterns of bands (+/+; +/-; -/-) for specimens that were previously identified as S. b. peruviensis. So again, if the AluTA15 was inserted into the ancestral lineage of S. boliviensis, as proposed by Osterholz et al. (2008)Osterholz M, Vermeer J, Walter L and Roos C (2008) A PCR-based marker to simply identify Saimiri sciureus and S. boliviensis boliviensis. Am J Primatol 70:1177-1180., it is unclear how specimens of this species could lack the insertion (-/-).

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Table 2
Presence (+) or absence (-) of the Alu TA15 insertion in the Saimiri specimens analyzed in the present study.

It is well known that Alu elements are replicated in a copy-and-paste way in the primate genome, and once inserted into a genome, they cannot be excised. Given this, individuals phenotypically typical of Saimiri b. peruviensis, but heterozygous for the insertion (+/-), must be the result of natural hybridization, which would presumably have involved the geographically closest taxon, S. sciureus macrodon. Furthermore, the absence of the insertion (-/-) in morphologically typical S. b. peruviensis can only be accounted for by the crossing of hybrid (+/-) Saimiri b. peruviensis or crosses between a hybrid and S. sciureus macrodon (-/-). These crosses would generate 25% or 50% of descendants without the insertion (-/-) and with dubious or intermediate morphological characteristics, which would represent conclusive evidence that hybridization between S. boliviensis and Saimiri sciureus macrodon produces fertile offspring. However, only 10% of the 50 Saimiri b. boliviensis specimens were heterozygous (+/-), and probably originated from crosses with Saimiri ustus, due to the proximity of the geographical distribution of these species (Figure 2).

It is interesting to note that S. b. peruviensis and S. s. macrodon occur sympatrically in the region between the Marañón and Tapiche rivers in the Peruvian Amazonia, whereas S. b. boliviensis is parapatric with S. s. macrodon and S. ustus, which are separated by the Juruá and Purus-Guaporé Rivers, respectively (Hershkovitz, 1984Hershkovitz P (1984) Taxonomy of squirrel monkeys genus Saimiri (Cebidae, Platyrrhini): A preliminary report with description of a hitherto unnamed form. Am J Primatol 6:257-312.). However, these rivers do not constitute an effective geographic barrier to gene flow in lizards (Souza et al., 2013Souza SM, Rodrigues MT and Cohn-Haft M (2013) Are Amazonia rivers biogeographic barriers for lizards? A study on the geographic variation of the spectacled lizard Leposoma osvaldoi Ávila-Pires (Squamata, Gymnophthalmidae). J Herpetol 47:511-519.), primates, and other organisms (Gascon et al., 2000Gascon C, Malcolm JR, Patton JL, Da Silva MN, Bogart JP, Lougheed SC, Peres CA, Neckel S and Boag PT (2000) Riverine barriers and the geographic distribution of Amazonian species. Proc Natl Acad Sci U.S.A. 97:13672-13677.), which implies that there may be gene flow between the present-day ranges of the three Saimiri species, resulting in hybridization between Saimiri boliviensis and Saimiri sciureus or S. ustus, as suggested by previous authors (Hershkovitz, 1984Hershkovitz P (1984) Taxonomy of squirrel monkeys genus Saimiri (Cebidae, Platyrrhini): A preliminary report with description of a hitherto unnamed form. Am J Primatol 6:257-312.; Thorington Jr, 1985Thorington Jr RW (1985) The taxonomy and distribution of squirrel monkeys (Saimiri). In: Rosenblum LA and Coe CL (eds) Handbook of Squirrel Monkey Research. Springer, New York, pp 1-33.; Silva et al., 1992Silva BTF, Sampaio MIC, Schneider H, Schneider MPC, Montoya E, Encarnacion F and Salzano FM (1992) Natural hybridization between Saimiri taxa in the Peruvian Amazonia. Primates 33:107-113., 1993Silva BTF, Sampaio MIC, Schneider H, Schneider MPC, Montoya E, Encarnacion F, Callegari Jacques SM and Salzano FM (1993) Protein electrophoretic variability in Saimiri and the question of its species status. Am J Primatol 29:183-193.; Osterholz et al., 2008Osterholz M, Vermeer J, Walter L and Roos C (2008) A PCR-based marker to simply identify Saimiri sciureus and S. boliviensis boliviensis. Am J Primatol 70:1177-1180.) based on morphological data.

Using chromosomal data, Jones and Ma (1975)Jones TC and Ma NSF (1975) Cytogenetics of the squirrel monkey (Saimiri sciureus). In: Goodwin WJ and Augustine J (eds) Primate Research. Springer, Boston, pp 13-21. were able to distinguish between S. b. peruviensis and S. s. macrodon from the vicinity of Iquitos (Peru) and Leticia (Colombia), respectively. Both species revealed a diploid number of 2n=42, with 10 meta/submetacentric, 22 acrocentric and 10 telocentric chromosomes in S. b. peruviensis, and 10 meta/submetacentric, 20 acrocrentic, and 12 telocentric chromosomes in S. s. macrodon. A hybrid produced in the laboratory between a male from Iquitos and a female from Leticia showed 10 meta/submetacentric, 11 acrocentic and 11 telocentric chromosomes. Lau and Arrighi (1976)Lau Y-F and Arrighi FE (1976) Studies of the squirrel monkey, Saimiri sciureus, genome 1. Cytological characterization of chromosomal heterozygosity. Cytogenet Cell Genet 17:51-60. using chromosomal banding analyses detected two nonhomologous pericentric inversions in the telocentric group of chromosomes of a squirrel monkey, Saimiri sciureus, suggesting that this individual was an intersubspecific hybrid whose parents originated from different geographical locations. Recently, Ruiz-García et al. (2015)Ruiz-García M, Luengas-Villamil K, Leguizamon N, De Thoisy B and Gálvez H (2015) Molecular phylogenetics and phylogeography of all the Saimiri taxa (Cebidae, Primates) inferred from mt COI and COII gene sequences. Primates 56:145-161. also found evidence of hybridization between Saimiri species based on mitochondrial markers (Cox1 and Cytb), emphasizing the importance of this process in the species-level diversification of this genus. In fact, these authors concluded that this genus comprises only three species, S. oerstedi, S. sciureus, and Saimiri vanzolinii, which diversified during the Pleistocene. This is consistent with the estimate of Alfaro et al. (2015)Alfaro JWL, Boubli JP, Paim FP, Ribas CC, Da Silva MNF, Messias MR, Röhe F, Mercês MP, Júnior JSS and Silva CR (2015) Biogeography of squirrel monkeys (genus Saimiri): South-central Amazon origin and rapid pan-Amazonian diversification of a lowland primate. Mol Phylogenet Evol 82:436-454., who concluded that S. boliviensis diverged from the other Saimiri species less than 1.5 Ma.

Hybridization may be a catalyst not only for speciation but also for major evolutionary innovations (Mallet (2007)Mallet J (2007) Hybrid speciation. Nature 446:279-283.. Hybridization between Saimiri species appears to be common, and as Mallet (2007)Mallet J (2007) Hybrid speciation. Nature 446:279-283. concludes at page 182: "most speciation involves natural selection; natural selection requires genetic variation; genetic variation is enhanced by hybridization; and hybridization and introgression between species is a regular occurrence, especially in rapidly radiating groups". On the basis of the evidence presented here, this appears to have been the case in Saimiri.

Acknowledgments

This study was part of the MSc thesis of JC, which was supported by the Brazilian National Council for Scientific and Technological Development (CNPq). This research was also supported by the collaborative program,Dimensions US-Biota-São Paulo: Assembly and evolution of the Amazon biota and its environment: an integrated approach, supported by the US National Science Foundation (NSF), National Aeronautics and Space Administration (NASA), and the São Paulo State Research Foundation (FAPESP). Funds for this research were also provided by CNPq (grants 306233/2009-6 to IS, and 473341/2010-7, 305645/2009-9) and CAPES Program No. 3296/2013-PROAM to HS

References

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  • Arnold ML and Meyer A (2006) Natural hybridization in primates: One evolutionary mechanism. Zoology 109:261-276.
  • Batzer MA and Deininger PL (2002) Alu repeats and human genomic diversity. Nat Rev Genet 3:370-379.
  • Chiou KL, Pozzi L, Alfaro JWL and Di Fiori A (2011) Pleistocene diversification of living squirrel monkeys (Saimiri spp) inferred from complete mitochondrial genome sequences. Mol Phylogenet Evol 59:736-745.
  • Costello RK, Dickinson C, Rosenberger AL, Boinski S and Szalay FS (1993) Squirrel monkey (genus Saimiri) taxonomy. In: Kimble WH and Martin LB (eds) Species, Species Concepts and Primate Evolution. Springer, Boston, pp 177-210.
  • Fearnside MP (2005) Brazil's Samuel Dam: Essons for hydro-electric development policy and the environment in Amazonia. Environ Manag 35:1-19.
  • Gascon C, Malcolm JR, Patton JL, Da Silva MN, Bogart JP, Lougheed SC, Peres CA, Neckel S and Boag PT (2000) Riverine barriers and the geographic distribution of Amazonian species. Proc Natl Acad Sci U.S.A. 97:13672-13677.
  • Genovart M (2009) Natural hybridization and conservation. Biodiv Conserv 18:1435-1439.
  • Hall TA (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95-98.
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  • Hershkovitz P (1984) Taxonomy of squirrel monkeys genus Saimiri (Cebidae, Platyrrhini): A preliminary report with description of a hitherto unnamed form. Am J Primatol 6:257-312.
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  • Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecology Evol 20:229-237.
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  • Matauschek C, Roos C and Heymann EW (2011) Mitochondrial phylogeny of tamarins (Saguinus, Hoffmannsegg 1807) with taxonomic and biogeographic implications for the S. nigricollis species groupAm J Phys Anthropol 144:564-574.
  • Osterholz M, Vermeer J, Walter L and Roos C (2008) A PCR-based marker to simply identify Saimiri sciureus and S. boliviensis boliviensis Am J Primatol 70:1177-1180.
  • Rieseberg LH (1997) Hybrid origins of plant species. Annu Rev Ecol Syst 28:359-389.
  • Ruiz-García M, Luengas-Villamil K, Leguizamon N, De Thoisy B and Gálvez H (2015) Molecular phylogenetics and phylogeography of all the Saimiri taxa (Cebidae, Primates) inferred from mt COI and COII gene sequences. Primates 56:145-161.
  • Salem A-H, Ray DA, Xing J, Callinan PA, Myers JS, Hedges DJ, Garber RK, Witherspoon DJ, Jorde LB and Batzer MA (2003) Alu elements and hominid phylogenetics. Proc Natl Acad Sci U S A 100:12787-12791.
  • Schreiber A, Wang M and Kaumanns W (1998) Captive breeding of squirrel monkeys, Saimiri sciureus and Saimiri boliviensis: the problem of hybrid groups. Zoo Biol 17:95-109.
  • Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecology Evol 19:198-207.
  • Shedlock A and Okada N (2000) SINE insertions: Powerful tools for molecular systematic. Bioessays 22:148-160.
  • Silva BTF, Sampaio MIC, Schneider H, Schneider MPC, Montoya E, Encarnacion F, Callegari Jacques SM and Salzano FM (1993) Protein electrophoretic variability in Saimiri and the question of its species status. Am J Primatol 29:183-193.
  • Silva BTF, Sampaio MIC, Schneider H, Schneider MPC, Montoya E, Encarnacion F and Salzano FM (1992) Natural hybridization between Saimiri taxa in the Peruvian Amazonia. Primates 33:107-113.
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  • Associate Editor: Francisco Mauro Salzano

Publication Dates

  • Publication in this collection
    31 Oct 2016
  • Date of issue
    Oct-Dec 2016

History

  • Received
    01 May 2016
  • Accepted
    11 Aug 2016
Creative Common - by 4.0
License information: This is an open-access article distributed under the terms of the Creative Commons Attribution License (type CC-BY), which permits unrestricted use, distribution and reproduction in any medium, provided the original article is properly cited.
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