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Genetic Variation of Mantled Howler Monkeys (Alouatta Palliata) from Costa Rica1

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Genetic Variation of Mantled Howler Monkeys (Alouatta Palliata) from Costa Rica1 BIOTROPICA 35(3): 375±381 2003 Genetic Variation of Mantled Howler Monkeys (Alouatta palliata) from Costa Rica1 Maria E. Zaldivar 2 Universidad de Costa Rica, Escuela de BiologõÂa, Ciudad Universitaria Rodrigo Facio, San Jose, Costa Rica Kenneth E. Glander Department of Biological Anthropology and Anatomy, Duke University, Durham, North Carolina 27708, U.S.A. Oscar Rocha, Gabriel Aguilar, Elida Vargas, Gustavo A. Gutierrez-Espeleta Universidad de Costa Rica, Escuela de BiologõÂa, Ciudad Universitaria Rodrigo Facio, San Jose, Costa Rica and Ronald Sanchez Universidad de Costa Rica, Departamento de Biologia, Sede Regional de Occidente, San RamoÂn, Costa Rica ABSTRACT We examined genetic diversity of howler monkeys (Alouatta palliata) from Costa Rica. Blood samples of howler monkeys were collected at various locations in Costa Rica, and electrophoresis of total plasma proteins yielded no variation. We also conducted starch gel electrophoresis of red cell isozymes and did not ®nd variation for any of the 14 loci analyzed (i.e., ACP, ADA, CA2, EST, GPI, IDH, LDH-1, LDH-2, MDH, PGD, PGM-1, PGM-2, SOD, and TPI). These ®ndings were compared with the levels of genetic variation for A. seniculus and A. belzebul from one Brazilian population. Four of the 14 isozymes (ADA, GPI, PGD, and SOD) showed more than one allele for these species. Both A. seniculus and A. belzebul from Brazil showed similar levels of genetic variation. The potential causes of the low genetic variation in A. palliata from Costa Rica are discussed. RESUMEN Se estudio la diversidad geneÂtica de los monos congo (Alouatta palliata) de Costa Rica. Se recolectaron muestras de sangre en varias localidades de Costa Rica. El anaÂlisis de las proteõÂnas totales del plasma mediante electroforesis no mostro variacioÂn. El anaÂlisis de las isoenzimas de gloÂbulos rojos mediante electroforesis en geles de almidoÂn tampoco mostro variacioÂn para ninguno de los 14 loci analizados (i.e., ACP, ADA, CA2, EST, GPI, IDH, LDH-1, LDH-2, MDH, PGD, PGM-1, PGM-2, SOD, y TPI). Estos resultados se compararon con los niveles de variacioÂn geneÂtica en A. seniculus y A. belzebul de una poblacioÂn de Brasil. Estas especies presentaron maÂs de un alelo en 4 de las 14 isoenzimas analizadas (ADA, GPI, PGD, y SOD). Tanto A. seniculus como A. belzebul presentaron niveles comparables de variacioÂn geneÂtica. Se discuten las causas potenciales de la poca variacioÂn geneÂtica en A. palliata de Costa Rica. Key words: dispersal; habitat fragmentation; howler monkeys; isozymes; New World monkeys. CENTRAL AMERICAN HOWLERS (ALOUATTA PALLIATA It has been proposed that the low genetic di- AND A. PIGRA) EXHIBIT EXTREMELY LOW LEVELS OF GE- versity of Central American howlers is due to the NETIC VARIATION for plasma proteins and red cell iso- action of random genetic drift (Froelich & Tho- zymes (Malmgren & Brush 1978, Froelich & Tho- rington 1982, Pope 1996, James et al. 1997). Ran- rington 1982, James et al. 1997). This observation dom genetic drift leads to the loss of genetic di- contrasts markedly with the high levels of genetic versity within populations (Falconer 1989; Futuy- variation shown by howler species from South ma 1989; Ellstrand & Elam 1993). Under these America (A. seniculus, A. belzebul, and A. fusca; Lima circumstances, we would expect to ®nd little or no et al. 1990, Pope 1992, Sampaio et al. 1996). variation within populations. This was the case for the populations described by Malmgren and Brush (1978), Froelich and Thorington (1982), and 1 Received 28 May 2002; revision accepted 24 August 2003. James et al. (1997), and for those reviewed by Pope 2 Corresponding author: Tel. (506) 207-4644, Fax (506) (1996). At the same time, random genetic drift 207-4216, e-mail: [email protected] promotes genetic differentiation between popula- 375 376 Zaldivar, Glander, Rocha, Aguilar, Vargas, Gutierrez-Espeleta, and Sanchez MATERIALS AND METHODS STUDY SPECIES. Mantled howlers (A. palliata)are one of the most variable of the six howler species, ranging in adult body size from 4.5 to 9.8 kg for males and 3.1 to 7.6 kg for females (Ford & Davies 1992). They are strict herbivores and eat mostly leaves and fruits from a variety of tree species, showing a very ¯exible diet (Glander 1978, 1981; Chapman 1987, 1990, Crockett & Eisenberg 1987). Mantled howlers are found from southern Mexico to northern Ecuador (Wolfheim 1983) and live in a wide variety of habitats, including decid- uous, riparian, evergreen, and montane forests (Crockett & Eisenberg 1987). They can occupy altered environments, including small patches of FIGURE 1. Location of study sites in Costa Rica, Cen- forest neighboring agricultural and urban areas. tral America. SAMPLE COLLECTION. Blood samples were collected from several mantled howler sites in Costa Rica tions since different alleles become ®xed in each during a period of four years, starting in 1993 (Fig. population (Falconer 1989, Futuyma 1989, Ells- 1). Table 1 lists the name of the site, the region trand & Elam 1993). Based on this, we would ex- within which it is located, and the number of sam- pect to ®nd variation between populations. This ples collected at each site. Most samples came from issue has not been addressed in previous research the Guanacaste region, located on the northwestern studies. side of the country. It has seasonal rains and veg- We conducted electrophoretic analyses for plas- etation typical of lowland deciduous and semi-de- ma proteins and red cell enzymes to characterize ciduous dry forests (Holdridge 1967, Janzen 1983). genetic variation in mantled howlers (A. palliata) The sample sites were: Santa Rosa National Park, from different sites within Costa Rica. We also did the largest protected area in the region; La Paci®ca, a comparative study between Costa Rican mantled a private cattle ranch, tourist resort, and forest re- howlers and Brazilian red howlers (A. seniculus) and serve (this population has been studied by KEG red-handed howlers (A. belzebul). The possible since 1970); Jimenez NunÄez, an agricultural station causes for the low levels of genetic variation in Cos- with a small forest reserve at the time of the study; ta Rican mantled howlers (A. palliata) are dis- and Santa Cruz, a cattle ranch near the town of cussed. Santa Cruz. TABLE 1. Number of samples of Alouatta palliata from each location. Geographical Number of Species, Site coordinates samples A. palliata, Costa Rica 137 GUANACASTE La Paci®ca 108469N, 858139W 91 Jimenez NunÄez 108259N, 858129W 15 Santa Cruz 108259N, 858599W 10 Santa Rosa 108839N, 858619W 6 CENTRAL PACIFIC Rio Jesus 108039N, 848529W7 ATLANTIC 28 Millas, LimoÂn 108099N, 838389W 6 Cariari, LimoÂn 108379N, 838749W 1 Pocosol, San Carlos 108369N, 848659W 1 Genetic Variation of Mantled Howlers 377 The Atlantic Region, on the eastern side of the stained with Coomasie Blue. We used a medium- country, receives a greater amount of rainfall and weight molecular marker from Promega to identify the populations studied are from areas with vege- the size of the proteins analyzed. tation typical of lowland rain forests (Holdridge 1967, Janzen 1983). Blood samples were collected ANALYSIS OF RED CELL ISOZYMES. Red cell isozymes at three sites: La Suerte, a ®eld station and former were analyzed using standard starch gel electropho- cattle ranch; 28 Millas, a banana plantation; and resis following the methods described by Harris Pocosol, a cattle ranch. and Hopkinson (1978), Richardson et al. (1986), The Central Region included only one site, Rio and Lima et al. (1990). A total of 76 samples of Jesus. This site is at a higher elevation, with vege- A. palliata was analyzed; only 30 samples from La tation typical of premontane humid forests (Hol- Paci®ca were included in these analyses (Table 1). dridge 1967, Janzen 1983), and is highly disturbed. We also analyzed 10 samples of A. belzebul and 10 The troop sampled occupied a 5 ha fragment of samples of A. seniculus. We examined 14 loci, forest neighboring coffee plantations and pasture- namely ACP, ADA, CA2, EST, GPI, IDH, LDH- lands. 1, LDH-2, MDH, PGD, PGM-1, PGM-2, SOD, All sampled populations were located at least and TPI. We used 9±11 percent starch gels. All 30 km from each other, with the exception of Ji- electrophoreses were run overnight at constant volt- menez NunÄez and La Paci®ca, which were ca 15 age (60±75 volts). We followed the staining pro- km from each other. Also, the Atlantic and Paci®c cedures recommended by Harris and Hopkinson Regions are separated by a mountain range running (1978). For multiple loci in the same isozyme sys- along the center of the country in a north±south tem, the most anodal isozyme was arbitrarily num- direction. bered ``1,'' with the remaining loci numbered se- Samples were collected using standard dart gun quentially. The different alleles for each isozyme techniques (Glander et al. 1991). Animals were (locus) were identi®ed in a similar fashion; the anesthetized with Telazol (tilethamine hydrochlo- most anodal allele was arbitrarily identi®ed as ``A,'' ride and zolazepam hydrochloride) and 5 ml of with the remaining alleles identi®ed sequentially. blood was drawn from their femoral vein using a Genetic analyses were conducted using the pro- vacutainer with ICD (isocitrate dextrose) or EDTA gram POPGENE 1.31 (Yeh et al. 1999). Using the as an anticoagulant. Animals were allowed to re- data from the red cell isozyme electrophoresis, we cover and were then released at the site of capture. determined the levels of genetic diversity for each The samples were kept cold until processing in the species using common indicators, such as observed laboratory. Once in the laboratory, the blood sam- number of alleles, effective number of alleles, Nei's ples were centrifuged at low speed for ca 15 min- diversity index, and the Shannon diversity index.
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