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Puerto Rico and Florida Manatees Represent Genetically Distinct Groups

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Puerto Rico and Florida Manatees Represent Genetically Distinct Groups Puerto Rico and Florida manatees represent genetically distinct groups Margaret E. Hunter, Antonio A. Mignucci-Giannoni, Kimberly Pause Tucker, Timothy L. King, Robert K. Bonde, Brian A. Gray, et al. Conservation Genetics ISSN 1566-0621 Conserv Genet DOI 10.1007/s10592-012-0414-2 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Science +Business Media Dordrecht 2012 (outside the USA). This e-offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self-archive your work, please use the accepted author’s version for posting to your own website or your institution’s repository. You may further deposit the accepted author’s version on a funder’s repository at a funder’s request, provided it is not made publicly available until 12 months after publication. 1 23 Author's personal copy Conserv Genet DOI 10.1007/s10592-012-0414-2 RESEARCH ARTICLE Puerto Rico and Florida manatees represent genetically distinct groups Margaret E. Hunter • Antonio A. Mignucci-Giannoni • Kimberly Pause Tucker • Timothy L. King • Robert K. Bonde • Brian A. Gray • Peter M. McGuire Received: 10 January 2012 / Accepted: 24 September 2012 Ó Springer Science+Business Media Dordrecht 2012 (outside the USA) 2012 Abstract The West Indian manatee (Trichechus manatus) suggested reclassification of the species to a threatened or populations in Florida (T. m. latirostris) and Puerto Rico delisted status. However, the two populations are geo- (T. m. manatus) are considered distinct subspecies and are graphically distant, morphologically distinct, and habitat listed together as endangered under the United States degradation and boat strikes continue to threaten the Puerto Endangered Species Act. Sustained management and con- Rico population. Here, 15 microsatellite markers and servation efforts for the Florida subspecies have led to the mitochondrial control region sequences were used to determine the relatedness of the two populations and investigate the genetic diversity and phylogeographic organization of the Puerto Rico population. Highly diver- Electronic supplementary material The online version of this article (doi:10.1007/s10592-012-0414-2) contains supplementary gent allele frequencies were identified between Florida and material, which is available to authorized users. Puerto Rico using microsatellite (FST = 0.16; RST = 0.12 (P \ 0.001)) and mitochondrial (F = 0.66; A = 0.50 & ST ST M. E. Hunter ( ) Á R. K. Bonde (P \ 0.001)) DNA. Microsatellite Bayesian cluster analy- Sirenia Project, Southeast Ecological Science Center, U.S. Geological Survey, 7920 NW 71st Street, Gainesville, ses detected two populations (K = 2) and no admixture or FL 32653, USA recent migrants between Florida (q = 0.99) and Puerto e-mail: [email protected] Rico (q = 0.98). The microsatellite genetic diversity val- ues in Puerto Rico (H = 0.45; N = 3.9), were similar, M. E. Hunter Á R. K. Bonde Á P. M. McGuire E A Aquatic Animal Health Program, College of Veterinary but lower than those previously identified in Florida Medicine, University of Florida, PO Box 100136, (HE = 0.48, NA = 4.8). Within Puerto Rico, the mito- Gainesville, FL 32610, USA chondrial genetic diversity values (p = 0.001; h = 0.49) were slightly lower than those previously reported A. A. Mignucci-Giannoni Puerto Rico Manatee Conservation Center, Inter American (p = 0.002; h = 0.54) and strong phylogeographic struc- University of Puerto Rico, PO Box 361715, San Juan, ture was identified (FST global = 0.82; AST global = 0.78 PR 00936, USA (P \ 0.001)). The genetic division with Florida, low diversity, small population size (N = 250), and distinct K. P. Tucker Biology Department, Stevenson University, threats and habitat emphasize the need for separate pro- 1525 Greenspring Valley Road, Stevenson, MD 21153, USA tections in Puerto Rico. Conservation efforts including threat mitigation, migration corridors, and protection of T. L. King subpopulations could lead to improved genetic variation in Aquatic Ecology Branch, Leetown Science Center, U.S. Geological Survey, 11649 Leetown Road, Kearneysville, the endangered Puerto Rico manatee population. WV 25430, USA Keywords Microsatellite DNA Á Mitochondria DNA Á B. A. Gray Marine mammal Á Endangered species Á Distinct population Department of Pediatrics, Division of Genetics, College of Medicine, University of Florida, segment Á Landscape genetics Á Phylogenetics Á 4800 SW 35th Dr, Gainesville, FL 32608, USA Conservation genetics 123 Author's personal copy Conserv Genet Introduction manatee species (Vianna et al. 2006). Within Florida, no variation was identified in the mtDNA cytochrome b or the The West Indian manatee (Trichechus manatus) popula- control region (Bradley et al. 1993; Garcı´a-Rodrı´guez et al. tions located in Puerto Rico (T. m. manatus) and Florida, 1998). The single Florida control region haplotype (A01) USA (T. m. latirostris) are recognized as distinct subspecies was also identified in the Puerto Rico population, along with based on morphological data, and are listed and managed two others, A02 and B01 (Garcı´a-Rodrı´guez et al. 1998; together as endangered under the U.S. Endangered Species Vianna et al. 2006). Since the two populations contain the Act (U.S. Fish and Wildlife Service 1982; Domning and same haplotype, they may be related through past or present Hayek 1986; Domning 1994, 2005). Habitat loss and high gene flow, or genetic drift in the mitochondrial control anthropogenic and natural mortality rates are threats to the region. Alternatively, they may be related through a common species (Mignucci-Giannoni et al. 2000; Lefebvre et al. ancestor and experiencing incomplete lineage sorting. 2001; Reep and Bonde 2006). Sustained management and Indeed, Florida is believed to have been colonized by man- conservation efforts in Florida have resulted in population atees from the Greater Antillean islands (Cuba, Jamaica, growth and a recommendation to reclassify West Indian Hispaniola, and Puerto Rico) as they moved northward after manatees from both populations to a threatened or delisted the last glacial event, approximately 12,000 years ago status (U.S. Fish and Wildlife Service 2007). To date, only (Domning 2005). mitochondrial DNA (mtDNA) data analyses have been used A limited number of studies have addressed nuclear DNA to assess the extent of migration and breeding between the (nDNA) diversity and population structure in manatees Florida and Puerto Rico manatee populations (Garcı´a- using microsatellites. The Florida subspecies (HE = 0.48, Rodrı´guez et al. 1998; Vianna et al. 2006). Furthermore, the NA = 4.8; 11 loci) indicated weak differentiation (FST = Puerto Rico Manatee Recovery Plan was drafted in 1986 0.02 (P \ 0.001) between the east and west coasts of Florida (Rathbun and Possardt 1986) and could benefit from an at 18 loci (Tucker et al. in press). The Belize manatee pop- updated threat assessment and conservation plan incorpo- ulation (HE = 0.46, NA = 3.4) was genetically divergent rating genetic data for improved recovery efforts. Micro- from Florida (FST = 0.14 (P \ 0.001)) at 16 loci and satellite DNA analyses were conducted here to provide showed evidence of two genetic clusters (Hunter et al. nuclear gene flow estimates for Florida and Puerto Rico. 2010a). At 13 loci, genetic differentiation (FST = 0.13 Treating these populations as one unit for management may (P \ 0.05)) was found between the Mexico population in not be advantageous, as the threats, habitat, population Chetumal Bay (HE = 0.46, NA = 3.0), the Gulf of Mexico sizes, and recovery efforts differ for the two populations. (HE = 0.41; NA = 2.7), and with Florida (FST = 0.10 The manatee population in Puerto Rico is estimated to (P \ 0.05); Nourisson et al. 2011). include 250 (170–360) individuals (Mignucci-Giannoni The diversity within Puerto Rico and the genetic rela- et al. 2000; Slone et al. 2006). From 1990 to 2006 a carcass tionship with other populations has been calculated using recovery program determined that anthropogenic mortality the mtDNA control region; however, no accompanying (28.9 % of all mortality) was caused by watercraft strike population structure information was provided (Garcı´a- (19.8 %), poaching (4.1 %), pollution (1.7 %), gunshot Rodrı´guez et al. 1998; Vianna et al. 2006). Mitochondrial (1.7 %), and drowning or entanglement (1.6 %; Bonde et al. DNA is maternally inherited and provides only information 2012). Analogous to Florida, watercraft related mortalities on the female genetic structure of the population at a single have recently become the leading cause of anthropogenic marker. Therefore, information from both mtDNA and mortality in Puerto Rico (Bonde et al. 2012; FWRI 2010). nDNA markers are used here to address the genetic struc- Further, a long-term study of Puerto Rico manatee deaths ture of both sexes and to increase the number of markers (1864–2006) revealed an overall increase in mortality dur- evaluating the population structure within Puerto Rico and ing the last 30 years of the study, rising an average of 9.6 % the relationship with Florida. per year (SD = 16.9 %; Mignucci-Giannoni et al. unpub- Genetic diversity is typically low in small populations lished data; Mignucci-Giannoni et al. 2000). Hunting of and can be quickly eroded during stochastic or demographic manatees for sustenance was documented from 1590–1995 events (Sherwin and Moritz 2000; Frankham et al. 2002). and likely contributed to the endangered status of the pop- Low diversity can also negatively influence fitness, ulation (Acosta 1590; Stahl 1883; Durand 1983; Mignucci- decrease population viability, and increase susceptibility to Giannoni et al. 2000). disease (O’Brien et al. 1983; Roelke et al. 1993). An inte- Overall, the West Indian manatee was found to have grative conservation approach uniting genetic and demo- similar mtDNA haplotype diversity (h = 0.86) and greater graphic information is needed to protect the biodiversity nucleotide diversity (p = 0.039) and number of polymor- available in small manatee populations and to sustain eco- phic sites (S = 45) than the Amazon (h = 0.88, p = 0.005, logical processes and evolutionary lineages.
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