Abstract
Three microsatellite loci were analyzed in ten remnant populations of silvery marmosets (Mico argentatus) in the fragmented landscape of central Amazonia, where surprisingly low levels of genetic diversity were observed (Ho = 0.11– 0.39). This pattern does not appear to be a result of habitat fragmentation, but rather of the ecological, behavioral, and reproductive characteristics of the species. Despite this, the results indicate that all the populations – including those resident in continuous forest – are subject to inbreeding and genetic drift. Overall, significant differentiation was found among populations (mean R st = 0.22, P < 0.001), which indicates that they are no longer part of the same gene pool. However, no correlation was observed between genetic and geographic distances among sites, which suggests that populations of these marmosets are not panmictic, even in large areas of continuous forest. In this case, in addition to inbreeding in small, isolated populations, the original genetic structure, characterized by a Whalund effect, may account for the high frequency of deviation from Hardy–Weinberg equilibrium found in the populations analyzed. For eventual conservation management, a primary recommendation would be to mitigate the effects of genetic drift by promoting gene flow among populations.
Resumen
Tres loci de microsatélites fueron analizados en diez poblaciones remanentes de la marmoseta plateada (Mico argentatus) en el paisaje fragmentado de la Amazonia central. Sorpresivamente se observaron niveles bajos de diversidad genética (Ho = 0.11– 0.39). Este patrón no parece ser el resultado de una fragmentación de hábitat, pero más bien de las características ecológicas, conductuales y reproductivas de la especie. A pesar de esto, los resultados indican que todas las poblaciones – incluyendo los residentes de bosques continuos – están sujetas a endogamia y deriva genética. De manera general, se encontraron diferencias genéticas significativas entre las poblaciones (R st medio = 0,22, P < 0,001), indicando que dichas poblaciones ya no son parte del mismo acervo genético. Sin embargo, no se observó una correlación entre las distancias genéticas y geográficas entre los sitios, lo cual sugiere que las poblaciones de estas marmosetas no son panmícticas, aún en áreas grandes de bosques continuos. En este caso, adicionalmente a la endogamia de las poblaciones pequeñas y aisladas, la estructura genética original está caracterizada por a efecto Whalund, el cual puede explicar la alta frecuencia de desviación del equilibrio Hardy–Weinberg encontrado en las poblaciones analizadas. Una recomendación primaria para el manejo para la conservación de la especie sería mitigar los efectos de la deriva genética promoviendo el flujo genético entre las poblaciones.
Resumo
Da análise de três loci microssatélites em dez populações de sagüis prateados (Mico argentatus) remanescentes de uma paisagem fragmentada da Amazônia Central, foi observada uma diversidade genética surpreendentemente baixa (Ho = 0,11 a 0,39). Este padrão não parece ser resultado da fragmentação de hábitat, mas de processos históricos relacionados principalmente às características ecológicas, comportamentais e reprodutivas da espécie. Por outro lado, os resultados indicam que todas as populações – incluindo aquela em floresta contínua – estão sujeitas ao endocruzamento e deriva genética. De maneira geral, foi observado um elevado e significante nível de diferenciação genética (R st médio = 0,22, P < 0,001), indicando que estas populações não fazem mais parte do mesmo pool gênico. Contudo, não foi observada correlação entre as distancias genética e geográfica entre populações, sugerindo, que mesmo em uma grande área contínua os sagüis não constituem uma população panmítica. Neste caso, em adição ao endocruzamento nas populações pequenas e isoladas, a estrutura genética original, com caracterização de efeito Wahlund, pode explicar a elevada freqüência do desvio do equilíbrio de Hardy–Weinberg nas populações levantadas. Para o eventual manejo conservacionista, recomenda-se principalmente a mitigação dos efeitos de deriva genética através da promoção de fluxo gênico entre as populações.
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Bastos HB (2007) Estrutura genética de Alouatta belzebul (Primates, Platyrrhini) da área de influência da UHE-Tucuruí. Masters Thesis, Universidade Federal do Pará, Belém
Benirschke K, Anderson JM, Brownhill LE (1962) Marrow chimerism in marmosets. Science 138:513–515
Callen DF, Thompson AD, Shen Y, Phillips HA, Richards RI, Mulley JC, Sutherland GR (1993) Incidence and origin of “null” alleles in the (AC) n microsatellite markers. Am J Hum Genet 52:922–927
Carvalho AN, Corrêa HKM, Coutinho PEG, Ferrari SF (2005) Composição de grupos de Mico argentatus (Callitrichinae, Primates) em um fragmento florestal na Amazônia Central. Resumos do XI Congresso Brasileiro de Primatologia. Sociedade Brasileira de Primatologia, Porto Alegre, p 85
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
Corrêa HKM (2006) Ecologia de grupos de Mico argentatus em fragmentos florestais naturais na Amazônia central. Doctoral Dissertation, Goeldi Museum, Belém
Dietz JM, Baker AJ, Ballou JD (2000) Demographic evidence of inbreeding depression in wild golden lion tamarins. In: Young AG, Clarke GM (eds) Genetics, demography, and the viability of fragmented populations. Cambridge University Press, Cambridge, pp 203–211
DiRienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA 91:3166–3170
Dixson AF, Anzenberger G, Monteiro da Cruz MAO, Patel I, Jeffreys AJ (1992) DNA fingerprinting of free-ranging groups of common marmosets (Callithrix jacchus jacchus) in NE Brazil. In: Martin RD, Dixson AF, Wickings EJ (eds) Paternity in primates: genetic tests and theories. Basel, Karger, pp 192–202
Dudash MR, Fenster CB (2000) Inbreeding and outbreeding depression in fragmented populations. In: Young AG, Clarke GM (eds) Genetics, demography, and the viability of fragmented populations. Cambridge University Press, Cambridge, pp 35–53
Ferrari SF (1993) Ecological differentiation in the callitrichidae. In: Rylands AB (ed) Marmosets and tamarins. systematics, behaviour, and ecology. Oxford University Press, Oxford, pp 314–328
Ferrari SF, Iwanaga S, Ravetta AL, Freitas FC, Sousa BAR, Souza LL, Costa CG, Coutinho PEG (2003) Dynamics of primate communities along the Santarém-Cuiabá highway in southern central Brazilian Amazônia. In: Marsh LK (ed) Primates in fragments. Kluwer, New York, pp 123–144
Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge
Gagneux P, Boesch C, Woodruff DS (1997) Microsatellite scoring errors associated with noninvasive genotyping based on nuclear DNA amplified from shed hair. Mol Ecol 6:861–868
Gonçalves EC, Ferrari SF, Silva A, Coutinho PEG, Menezes EV, Schneider MPC (2003) Effects of habitat fragmentation on the genetic variability of silvery marmosets, Mico argentatus. In: Marsh LK (ed) Primates in fragments. Kluwer, New York, pp 17–28
Goodman SJ (1997) Rst calc: a collection of computer programs for calculating estimates of genetic differentiation from microsatellite data and determining their significance. Mol Ecol 6:881–885
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indexes. Version 2.9.3. http://www.unil.ch/izea/softwares/fstat.html
Grativol AD, Ballou JD, Fletcher R (2001) Microsatellite variation within and among recently isolated populations of golden lion tamarins. Conserv Genet 2:1–9
Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725–738
Lacy RC (1997) Importance of genetic variation to the variability of mammalian populations. J Mammal 78:320–335
Luikart G, Cornuet J-M (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237
Marsh LK (2003) Primates in fragments. Kluwer, New York
Melo MAD (2004) Variabilidade e estrutura genética em três populações naturais de Aotus infulatus da Amazonia oriental. Masters Thesis, Universidade Federal do Pará, Belém
Miranda IS (1993) Estrutura do estrato arbóreo do cerrado amazônico de Alter do Chão, Pará, Brasil. Rev Bras Bot 16:143–150
Nievergelt CM, Mundy NI, Woodruff DS (1998) Microsatellite primers for genotyping common marmosets (Callithrix jacchus) and other callitrichids. Mol Ecol 5:1432–1434
Ohta T, Kimura M (1973) A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a finite population. Genet Res 22:201–204
Piry S, Luikart G, Cornuet J-M (1999) BOTTLENECK 1202: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503
Pope TR (1996) Socioecology, population fragmentation, and patterns of genetic loss in endangered primates. In: Avise JC, Hamrick JL (eds) Conservation genetics: case histories from nature. Chase & Hall, New York, pp 119–159
Pope TR (1998) Genetic variation in remnant populations of the woolly spider monkey (Brachyteles arachnoides). Int J Primatol 19:95–109
Raymond M, Rousset F (1995) Genepop version 1.2: population genetics software for exact tests and ecumenism. J Hered 86:248–249
Rylands AB (1986) Ranging behaviour and habitat preference of a wild marmoset group, Callithrix humeralifer (Callitrichidae, Primates). J Zool Lond 210:489–514
Rylands AB, Schneider H, Langguth A, Mittermeier RA, Groves CP, Rodriguez-Luna E (2000) An assessment of the diversity of New World primates. Neotrop Primates 8:61–93
Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462
Strier KB (2000) Primate behavioral ecology. Allyn and Bacon, Boston
Tavares LI (1999) Estratégias de Forrageio de Callithrix argentata (Linnaeus 1771) na Estação Científica Ferreira Penna, Pará. Masters Thesis, Universidade Federal do Pará, Belém
Tavares LI, Ferrari SF (2002) Diet of the silvery marmoset (Callithrix argentata) at ECFPn: seasonal and longitudinal variation. In: Lisboa PLB (ed) Caxiuanã: Biodiversidade e Sustentabilidade. CNPq, Belém, pp 707–719
Templeton AR (1986) Coadaptation and outbreeding depression. In: Soulé ME (ed) Conservation biology: the science of scarcity and diversity. Sinauer, Sunderland, pp 105–116
Templeton AR, Read B (1983) The elimination of inbreeding depression in a captive herd of Speke’s gazelle. In: Schonewald-Cox CM, MacBryde B, Thomas L (eds) Genetics and conservation. Benjamin Cummings Inc., Menlo Park, CA, pp 241–261
van Roosmalen MGM, van Roosmalen T, Mittermeier RA, Rylands AB (2000) Two new species of marmoset, genus Callithrix Erxleben, 1777 (Callitrichidae, Primates) from the Tapajós-Madeira interfluvium, saouth Central Amazonia, Brazil. Neotrop Primates 8:2–19
Veracini C (this volume) Habitat use and ranging behavior of the silvery marmoset (Mico argentatus) at Caxiuanã National Forest (eastern Brazilian Amazonia). In: Ford SM, Porter LM, Davis LC (eds) The smallest anthropoids: the marmoset/callimico radiation. Springer, New York, pp 221–240
Yeh FC, Yang RC, Boylet T (1997) POPGENE (version 1.32): Software microsoft window-based freeware for population genetic analysis. University of Alberta, Canada
Acknowledgments
This study was part of the Brazilian Environment Ministry’s PROBIO initiative, financed by BIRD and CNPq, with additional support from FINEP/PRONEX, IBAMA/Santarém and the Kapok Foundation. The collection of specimens was authorized by IBAMA through special license 157/2001-DIFAS/DIREC. We are grateful to Adenilson Carvalho, Wellton Costa and Caroline Nievergelt for their help with data collection and analysis.
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Gonçalves, E., Ferrari, S.F., Coutinho, P.E.G., Menezes, E., Silva, A., Schneider, M.P.C. (2009). Limited Dispersal and Genetic Structure of Silvery Marmosets (Mico argentatus) in the Fragmented Landscape of Central Amazonia. In: Ford, S., Porter, L., Davis, L. (eds) The Smallest Anthropoids. Developments in Primatology: Progress and Prospects. Springer, Boston, MA. https://doi.org/10.1007/978-1-4419-0293-1_11
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