Abstract
The ecology of a species strongly influences genetic variation and population structure. This interaction has important conservation implications because taxa with low dispersal capability and inability to use different habitats are more susceptible to anthropogenic stressors. Ocelots (Leopardus pardalis albescens) and bobcats (Lynx rufus texensis) are sympatric in Texas and northeastern Mexico; however, their ecology and conservation status are markedly different. We used 10 microsatellite loci and a 397-bp segment of the mitochondrial control region to examine how historical and ecological differences in these two species have influenced current patterns of genetic diversity in a landscape heavily altered by anthropogenic activities. Substantially higher genetic diversity (heterozygosity and haplotype diversity) and population connectivity was observed for bobcats in comparison to ocelots. The level of divergence among proximate ocelot populations (<30 km) was greater than between bobcat populations separated by >100 km. Ocelot populations in the US have never recovered from reductions experienced during the twentieth century, and their low genetic variation and substantial isolation are exacerbated by strong preference for dense native thornshrub and avoidance of open habitat. In contrast, despite continued legal harvesting and frequent road-related mortality, bobcats have maintained wide distribution, high abundance, and population connectivity. Our study illustrates that sympatric species with a similar niche can still have sufficient ecological differences to alter their response to anthropogenic change. Sensitive species, such as the ocelot, require additional conservation actions to sustain populations. Ecological differences among species occupying a similar guild are important to consider when developing conservation plans.
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References
Avise JC (1994) Molecular markers, natural history, and evolution. Chapman & Hall, New York
Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge
Blankenship TL (2000) Ecological response of bobcats to fluctuating prey populations on the Welder Wildlife Foundation Refuge. Dissertation, Texas A&M University–Texas A&M University–Kingsville, College Station and Kingsville, Texas, USA
Blankenship TL, Haines AM, Tewes ME, Silvy NJ (2006) Comparing survival and cause-specific mortality between resident and transient bobcats Lynx rufus. Wildl Biol 12:297–304
Branch LC, Clark AM, Molar PE, Bowen BW (2003) Fragmented landscapes, habitat specificity, and conservation genetics of three lizards in Florida scrub. Conserv Genet 2:199–212
Büchi L, Vuilleumier S (2014) Coexistence of specialist and generalist species is shaped by dispersal and environmental factors. Am Nat 183:612–624
Casas-Marce M, Soriano L, Lopez-Bao JV, Godoy JA (2013) Genetics at the verge of extinction: insights from the Iberian lynx. Mol Ecol 22:5503–5515
Caso A (1994) Home range and habitat use of three neotropical carnivores in northeast Mexico. Thesis, Texas A&M University–Kingsville, Kingsville, USA
Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660
Crooks KR (2002) Relative sensitivities of mammalian carnivores to habitat fragmentation. Conserv Biol 16:488–502
Croteau EK, Heist EJ, Nielsen CK, Hutchinson JR, Hellgren EC (2012) Microsatellites and mitochondrial DNA reveal regional population structure in bobcats (Lynx rufus) of North America. Conserv Genet 13:1637–1651
Delaney KS, Riley SPD, Fisher N (2010) A rapid, strong, and convergent genetic response to urban habitat fragmentation in four divergent and widespread vertebrates. PLoS ONE 5(9):e12767. doi:10.1371/journal.pone.0012767
Didham RK (2010) Ecological consequences of habitat fragmentation. In: Janson R (ed) Encyclopedia of life sciences. Wiley, Chichester. doi:10.1002/9780470015902.a0021904
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491
Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50
Fisher CV (1998) Habitat use by free-ranging felids in an agroecosystem. Masters Thesis, Texas A&M University–Kingsville, Kingsville, USA
Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140
Frankham R, Ralls K (1998) Conservation biology: inbreeding leads to extinction. Nature 392:441–442
Freeman AR, MacHugh DE, McKeown S, Walzer C, McConnell DJ, Bradley DG (2001) Sequence variation in mitochondrial DNA control region of wild African cheetah (Acinonyx jubatus). Heredity 86:355–362
Fu XH, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709
Gårdmark A, Enberg K, Ripa J, Laasko J, Kaitala V (2003) The ecology of recovery. Ann Zool Fenn 40:131–144
Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
Gubbi S, Poornesha HC, Madhusudan MD (2012) Impact of vehicular traffic on the use of highway edges by large mammals in a South Indian wildlife reserve. Curr Sci 102:1047–1051
Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportions for multiple alleles. Biometrics 48:361–372
Haines AM, Tewes ME, Laack LL (2005a) Survival and sources of mortality in ocelots. J Wildl Manag 69:255–263
Haines AM, Tewes ME, Laack LL, Grant WE, Young JH (2005b) Evaluating recovery strategies for an ocelot population in southern Texas. Biol Conserv 126:512–522
Haines AM, Grassman LI Jr, Tewes ME, Janecka JE (2006a) The first ocelot (Leopardus pardalis) monitored via GPS telemetry. Eur J Wildl Res 52:216–218
Haines AM, Janecka JE, Tewes ME, Grassman LI Jr (2006b) The importance of private lands for the endangered ocelot Leopardus pardalis in the United States using camera traps. Oryx 40:1–5
Haines AM, Tewes ME, Laack LL, Horne JS, Young JH (2006c) A habitat-based population viability analysis for ocelots (Leopardus pardalis) in the United States. Biol Conser 132:424–436
Haines AM, Leu M, Svancara L, Wilson G, Scott JM, Reese KP (2008) A theoretical approach to using human footprint models to measure landscape level conservation success. Conserv Lett 1:165–172
Harveson PM, Tewes ME, Anderson GL, Laack LL (2004) Habitat use by ocelots in south Texas: implications for restoration. Wildl Soc Bull 32:948–954
Hedrick P (2011) Genetics of populations, 4th edn. Jones and Barlett Publishers, Sudbury
Heilbrun RD, Silvy NJ, Peterson MJ, Tewes ME (2006) Estimating bobcat abundance using automatically triggered cameras. Wildl Soc Bull 34:69–73
Henle K, Davies KF, Kleyer M, Margules C, Settele J (2004) Predictors of species sensitivity to fragmentation. Biodivers Conserv 13:207–251
Homer C, Dewitz J, Fry J, Coan M, Hossain N, Larson C, Herold N, McKerrow A, VanDriel JN, Wickham J (2007) Completion of the 2001 National Land Cover Database for the Conterminous United States. Photogramm Eng Remote Sens 73(4):337–341
Horne JS, Haines AM, Tewes ME, Laack LL (2009) Habitat partitioning by sympatric ocelots and bobcats: implications for recovery of ocelots in southern Texas. Southwest Nat 54:119–126
Jackson VL, Zimmerman EG (2005) Landscape metrics associated with habitat use by ocelots in south Texas. J Wildl Manag 69:733–738
Jae-Heup K, Eizirik E, O’Brien SJ, Johnson WE (2001) Structure and patterns of sequence variation in the mitochondrial DNA control region of the great cats. Mitochondrion 14:279–292
Jahrsdoerfer SE, Leslie DM Jr (1988) Tamaulipan brushland of the Lower Rio Grande Valley of South Texas: description, human impacts, and management options. United States fish and wildlife service. Biol Rep 88(36):66
Janecka JE, Blankenship TL, Hirth DH, Tewes ME, Kilpatrick CW, Grassman LI Jr (2006a) Kinship and social structure of bobcats (Lynx rufus) inferred from microsatellite and radio-telemetry data. J Zool (London) 269:494–501
Janecka JE, Grassman LI Jr, Derr JN, Honeycutt RL, Eiadthong W, Tewes ME (2006b) Rapid whole genome amplification of DNA from felids: applications for conservation genetics. Wildl Soc Bull 34:1134–1141
Janecka JE, Blankenship TL, Hirth DH, Kilpatrick CW, Grassman LI Jr, Tewes ME (2007a) Evidence for male-biased dispersal in bobcats using relatedness and kinship analysis. J Wildl Biol 13:38–47
Janecka JE, Grassman LI Jr, Honeycutt RL, Tewes ME (2007b) Whole genome amplification for sequencing and applications in conservation genetics. J Wildl Manag 71:1357–1360
Janecka JE, Walker CW, Tewes ME, Caso A, Laack LL, Honeycutt RL (2007c) Phylogenetic relationships of ocelot (Leopardus pardalis albescens) populations from the Tamaulipan Biotic Province and implications for recovery. Southwest Nat 52:89–96
Janecka JE, Tewes ME, Grassman LI Jr, Haines AM, Honeycutt RL (2008) Small effective population sizes of two remnant ocelot populations (Leopardus pardalis albescens) in the United States. Conserv Genet 9:869–878
Janecka JE, Tewes ME, Laack LL, Caso A, Grassman LI Jr, Haines AM, Shindle DB, Davis B, Murphy WJ, Honeycutt RL (2011) Reduced genetic diversity and isolation of remnant ocelot populations occupying a severely fragmented landscape in southern Texas. Anim Conserv 14:608–619
Janecka JE, Tewes ME, Laack LL, Caso A, Grassman LI Jr, Honeycutt RL (2014) Loss of genetic diversity among ocelots in the United States during the 20th century linked to human induced population reductions. PLoS ONE 9(2):e89384:1–e89384:10
Laack LL (1991) Ecology of the ocelot (Felis pardalis) in south Texas. Masters Thesis, Texas A&I University, Kingsville, USA
Laack LL, Tewes ME, Haines AM, Rappole J (2005) Reproductive life history of ocelots Leopardus pardalis in southern Texas. Acta Theriol 50:505–514
Larivière S, Walton LR (1997) Lynx rufus. Mamm Species 563:1–8
Lee JS, Ruell EW, Boydston EE, Lyren LM, Alonso RS, Troyer JL, Crooks KR, VandeWoude S (2012) Gene flow and pathogen transmission among bobcats (Lynx rufus) in a fragmented urban landscape. Mol Ecol 21:1617–1631
MacArthur RH (1972) Geographical ecology. Princeton University Press, Princeton
Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220
Menotti-Raymond M, David VA, Lyons LA, Schaffer AA, Tomlin JF, Hutton MK, O’Brien SJ (1999) A genetic linkage map of microsatellites in the domestic cat (Felis catus). Genomics 57:9–23
Murray JL, Gardner GL (1997) Leopardus pardalis. Mamm Species 548:10–16
Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Nat Acad Sci USA 76:5269–5273
O’Brien SJ, Evermann JF (1988) Interactive influence of infectious disease and genetic diversity in natural populations. Trends Ecol Evol 3:254–259
O’Brien SJ, Roelke ME, Marker L, Newman A, Winkler CA, Meltzer D, Collym L, Evermann JF, Bush M, Wildt DE (1985) Genetic basis for species vulnerability in the cheetah. Science 227:1428–1434
O’Brien SJ, Martenson JS, Packer C, Herbst L, de Vos V, Joslin P, Ott-Joslin J, Wildt DE (1987) Biochemical genetic variation in geographic isolates of African and Asiatic lions. Nat Geogr Res 3:114–124
Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65
Palomares F, Godoy JA, Piriz A, O’Brien SJ, Johnson WE (2002) Faecal genetic analysis to determine the presence and distribution of elusive carnivores: design and feasibility for the Iberian lynx. Mol Ecol 11:2171–2182
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539
Price CV, Nakagaki NK, Hitt J, Clawges RC (2006) Enhanced historical land-use and land-cover data sets of the U.S. Geological Survey, U.S. Geological survey digital data series 240. [digital data set] http://pubs.usgs.gov/ds/2006/240
Pritchard JK, Stephens M, Donnely P (2000) Inference of population structure from multilocus data. Genetics 155:945–949
Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Nat Acad Sci USA 94:9197–9201
Reding DM, Bronikowski AM, Johnson WE, Clark WR (2012) Pleistocene and ecological effects on continental-scale genetic differentiation in the bobcat (Lynx rufus). Mol Ecol 21:3078–3093
Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237
Reed DH, Lowe EH, Briscoe DA, Frankham R (2003) Inbreeding and extinction: effects of rate of inbreeding. Conserv Genet 4:405–410
Rice JE (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Riley SPD, Sauvajot RM, Fuller TK (2003) Effects of urbanization and habitat fragmentation on bobcats and coyotes in southern California. Conserv Biol 17:566–576
Riley SPD, Pollinger JP, Sauvajot RM (2006) A southern California freeway is a physical and social barrier to gene flow in carnivores. Mol Ecol 15:1733–1741
Riley SPD, Boydston EE, Crooks KR, Lyren LM (2010) Bobcats (Lynx rufus). In: Gehrt SD, Riley SPD, Cypher BL (eds) Urban carnivores: ecology, conflict, and conservation. Johns Hopkins University Press, Baltimore, pp 121–138
Roelke ME, Martenson JS, O’Brien SJ (1993) The consequences of demographic reduction and genetic depletion in the endangered Florida panther. Curr Biol 3:340–350
Rogala JK, Hebblewhite M, Whittington J, White CA, Coleshill J, Musiani M (2011) Human activity differentially redistributes large mammals in the Canadian Rockies national parks. Ecol Soc 16:16
Rosenzweig ML (1981) A theory of habitat selection. Ecology 62:327–335
Rozas J, Rozas R (1999) DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174–175
Ruell EW, Riley SP, Douglas MR, Pollinger JP, Crooks KR (2009) Estimating bobcat population sizes and densities in a fragmented urban landscape using noninvasive capture-recapture sampling. J Mamm 90:129–135
Sanderson EW, Jaiteh M, Levy MA, Redford KH, Wannebo AV, Woolmer G (2002) The human footprint and the last of the wild. Bioscience 52:891–904
Schmidly DJ (2002) Texas natural history: a century of change. Texas Tech University Press, Lubbock
Schmidly DJ (2004) The mammals of Texas. University of Texas Press, Austin
Schmidt K, Kowalczyk R, Ozolins J, Männil P, Fickel J (2009) Genetic structure of the Eurasian lynx population in north-eastern Poland and the Baltic states. Conserv Genet 10:497–501
Shindle DB, Tewes ME (1998) Woody species composition of habitats used by ocelots (Leopardus pardalis) in the Tamaulipan Biotic Province. Southwest Natt 43:273–279
Shindle DB, Tewes ME (2000) Immobilization of wild ocelots with tiletamine and zolazepam in southern Texas. J Wildl Dis 36:546–550
Slatkin M, Barton NH (1989) A comparison of three indirect methods for estimating average levels of gene flow. Evolution 43:1349–1368
Sugg DW, Chesser RK, Dobson FS, Hoogland JL (1996) Population genetics meets behavioral ecology. Trends Ecol Evol 11:338–342
Sunquist ME, Sunquist F (2002) Wild cats of the world. University of Chicago Press, Chicago
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Tewes ME (1986) Ecological and behavioral correlates of ocelot spatial patterns. Dissertation, University of Idaho, Moscow, USA
Tewes ME, Everett DD (1986) Status and distribution of the endangered ocelot and jaguarundi in Texas. In: Miller SD, Everett DD (eds) Cats of the world: biology, conservation, and management. National Wildlife Federation, Washington, pp 147–158
Thompson JD, Gibson TJ, Plewniak F, Jean-Mougin F, Higgins DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Tremblay TA, White WA, Raney JA (2005) Native woodland loss during the mid 1900s in Cameron County, Texas. Southwest Nat 50:479–487
United States Census Bureau (2010) Census. http://www.census.gov. Accessed 3 March 2015
Uphyrkina O, Miquelle D, Quigley H, Driscoll C, O’Brien SJ (2002) Conserv genet of the Far Eastern leopard (Panthera pardus oreintalis). J Hered 93:303–311
Whittaker RJ (1998) Island biogeography: ecology, evolution, and conservation. Oxford University Press, Oxford
Wildt DE, Bush M, Goodrowe KL, Packer C, Pusey AE, Brown JL, Joslin P, O’Brien SJ (1987) Reproductive and genetic consequences of founding isolated lion populations. Nature 329:328–331
Acknowledgments
We thank the Rob and Bessie Welder Wildlife Foundation (to TLB and JEJ), Tim and Karen Hixon Foundation (to MET), Rachel and Ben Vaughan Foundation (to MET), James R. Dougherty Foundation (to MET), Karen and Phil Hunke (to MET), and Texas Parks and Wildlife Department Grant E-77-R (to JEJ & RLH) for funding this project. This article represents publication number 15-114 of the Caesar Kleberg Wildlife Research Institute, 001 of the East Wildlife Foundation, and 714 of the Rob and Bessie Welder Foundation. We thank Randy DeYoung, Alan Fedynich, and Mary Janecka for thorough editing of the manuscript and valuable comments, and Matt Jevit for creating species distribution map.
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Janecka, J.E., Tewes, M.E., Davis, I.A. et al. Genetic differences in the response to landscape fragmentation by a habitat generalist, the bobcat, and a habitat specialist, the ocelot. Conserv Genet 17, 1093–1108 (2016). https://doi.org/10.1007/s10592-016-0846-1
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DOI: https://doi.org/10.1007/s10592-016-0846-1