Conservation implications
As the only extant felids in Taiwan, leopard cats may play a crucial
role as apex predators, contributing to ecosystem stability and trophic
cascades (Pace et al., 1999; Terborgh et al., 1999). Our genetic study
complements previous ecological research (Chen et al., 2016; van der
Meer et al., 2023), revealing that direct and indirect impacts of
anthropogenic features have compromised the sustainability of Taiwanese
leopard cat populations. Although there is currently no evidence of
genetic drift or inbreeding affecting the genetic diversity among
leopard cat populations in Taiwan, human-related landscape features have
contributed to genetic differentiation among its populations. Despite no
prospect of significant loss of diversity in the near future, our
species distribution models predict that climate change may further
endanger the viability and connectivity of Taiwanese populations,
restricting suitable habitats to northern and mountainous regions with
rugged topography. The mitochondrial marker revealed extremely low
genetic diversity in the leopard cat populations of Taiwan. Indeed, it
is the lowest among related populations in Far East Asia (Ito &
Inoue-Murayama, 2019; Ko, An, & Eo, 2022; Teng et al., 2022). Moreover,
the distinct Taiwanese haplotypes indicate limited gene flow between
peripheral island habitats and continental core populations (Patel et
al., 2017; Tamada et al., 2008). The evolutionary potential to adapt to
changing environments depends on the balance between genetic variation
and drift (Brown, 1984; Holderegger, Kamm, & Gugerli, 2006; Slatkin,
1987). However, the low genetic variation resulting from founder effects
and lack of new genetic components increases the risk of local
extinctions in island populations facing extreme climate change
(Johnson, Adler, & Cherry, 2000; Wood et al., 2017).
The key conservation management actions for Taiwanese leopard cats
should focus on maintaining neutral and adaptive genetic diversity,
population fitness, and evolutionary potential in the face of habitat
fragmentation and impending climate alterations. Efforts should be made
to reduce adverse human activities that drive genetic differentiation in
the island’s leopard cats, such as establishing corridors to facilitate
gene flow between fragmented habitats. Protected areas can be designated
in areas of high dispersal potential to minimize disturbance from human
activities and predation by free-roaming domestic dogs. To mitigate
fragmentation and reduce the risk of road collisions, artificial
underground or aboveground corridors can be implemented along highways
in areas with a high population density of leopard cats. Lastly, to
counteract the negative effects of drift and inbreeding caused by
isolation and climate change, establishing corridors connecting southern
and northern areas should be a high priority to prevent loss of genetic
diversity and reduce the risk of local extinctions. Our study provides
valuable insights into how landscape features shape the evolutionary
processes and future distribution of a locally endangered felid on a
subtropical island, offering fundamental ecological information for its
conservation.
References
Adkins C, Stott P (1998) Home ranges, movements and habitat associations
of red foxes Vulpes vulpes in suburban Toronto, Ontario, Canada.Journal of Zoology, 244 (3), 335-346.
Barclay GW (2015) Colonial development and population in Taiwan(Vol. 2149): Princeton University Press.
Bazin E, Glémin S, Galtier N (2006) Population size does not influence
mitochondrial genetic diversity in animals. Science, 312 (5773),
570-572.
Bolliger J, Lander T, Balkenhol N (2014) Landscape genetics since 2003:
status, challenges and future directions. Landscape Ecology, 29 ,
361-366.
Brown JH (1984) On the relationship between abundance and distribution
of species. The American Naturalist, 124 (2), 255-279.
Castilho CS, Hackbart VC, Pivello VR, dos Santos RF (2015) Evaluating
landscape connectivity for Puma concolor and Panthera onca among
Atlantic forest protected areas. Environmental Management, 55 ,
1377-1389.
Chang Y, Chao M, Ding S, Lin EC, Tsao H, Yuan H, Wang P (2012)
Development of microsatellite markers in an ungulate mammal, the
Formosan serow (Capricornis swinhoei). Conservation Genetics
Resources, 4 , 755-757.
Chen CC, Chang AM, Wada T, Chen MT, Tu YS (2019) Distribution of
Carnivore protoparvovirus 1 in free-living leopard cats (Prionailurus
bengalensis chinensis) and its association with domestic carnivores in
Taiwan. PLoS One, 14 (9), e0221990.
Chen JS (1956) A Synopsis of the Vertebrates of Taiwan. Kaimin
Press, Taipei , 619 pp.
Chen MT, Liang YJ, Kuo CC, Pei KJC (2016) Home ranges, movements and
activity patterns of leopard cats (Prionailurus bengalensis) and threats
to them in Taiwan. Mammal Study, 41 (2), 77-86.
Clark RW, Brown WS, Stechert R, Zamudio KR (2010) Roads, interrupted
dispersal, and genetic diversity in timber rattlesnakes.Conservation biology, 24 (4), 1059-1069.
Clarke RT, Rothery P, Raybould AF (2002) Confidence limits for
regression relationships between distance matrices: estimating gene flow
with distance. Journal of Agricultural, Biological, and
Environmental Statistics , 361-372.
Cornuet JM, Pudlo P, Veyssier J et al. (2014) DIYABC v2. 0: a
software to make approximate Bayesian computation inferences about
population history using single nucleotide polymorphism, DNA sequence
and microsatellite data. Bioinformatics, 30 (8), 1187-1189.
Cushman SA, Landguth EL (2010) Spurious correlations and inference in
landscape genetics. Molecular Ecology, 19 (17), 3592-3602.
Cushman SA, Shirk AJ, Landguth EL (2013) Landscape genetics and limiting
factors. Conservation Genetics, 14 , 263-274.
Cushman SA, Wasserman TN, Landguth EL, Shirk AJ (2013) Re-evaluating
causal modeling with Mantel tests in landscape genetics.Diversity, 5 (1), 51-72.
Ding L, Gan XN, He SP, Zhao EM (2011) A phylogeographic, demographic and
historical analysis of the short‐tailed pit viper (Gloydius
brevicaudus): evidence for early divergence and late expansion during
the Pleistocene. Molecular Ecology, 20 (9), 1905-1922.
Ellstrand NC, Elam DR (1993) Population genetic consequences of small
population size: implications for plant conservation. Annual
review of Ecology and Systematics, 24 (1), 217-242.
Epps CW, Keyghobadi N (2015) Landscape genetics in a changing world:
disentangling historical and contemporary influences and inferring
change. Molecular Ecology, 24 (24), 6021-6040.
Epps CW, Palsbøll PJ, Wehausen JD, Roderick GK, Ramey RR, McCullough DR
(2005) Highways block gene flow and cause a rapid decline in genetic
diversity of desert bighorn sheep. Ecology letters, 8 (10),
1029-1038.
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of
individuals using the software STRUCTURE: a simulation study.Molecular Ecology, 14 (8), 2611-2620.
Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of
programs to perform population genetics analyses under Linux and
Windows. Molecular Ecology Resources, 10 (3), 564-567.
Fick SE, Hijmans RJ (2017) WorldClim 2: new 1‐km spatial resolution
climate surfaces for global land areas. International journal of
climatology, 37 (12), 4302-4315.
Frankel OH, Frankel O, Soulé ME (1981). Conservation and
evolution : CUP Archive.
Funk DJ, Omland KE (2003) Species-level paraphyly and polyphyly:
frequency, causes, and consequences, with insights from animal
mitochondrial DNA. Annual Review of Ecology, Evolution, and
Systematics, 34 (1), 397-423.
Fusco NA, Carlen EJ, Munshi-South J (2021) Urban landscape genetics: are
biologists keeping up with the pace of urbanization? Current
Landscape Ecology Reports, 6 , 35-45.
Goudet J (1995) FSTAT (version 1.2): a computer program to calculate
F-statistics. Journal of heredity, 86 (6), 485-486.
Grilo C, Bissonette JA, Santos-Reis M (2009) Spatial–temporal patterns
in Mediterranean carnivore road casualties: consequences for mitigation.Biological Conservation, 142 (2), 301-313.
Haffer J (1969) Speciation in Amazonian Forest Birds: Most species
probably originated in forest refuges during dry climatic periods.Science, 165 (3889), 131-137.
Holderegger R, Kamm U, Gugerli, F (2006) Adaptive vs. neutral genetic
diversity: implications for landscape genetics. Landscape Ecology,
21 , 797-807.
Hollander M, Wolfe DA, Chicken E (2013) Nonparametric statistical
methods : John Wiley & Sons.
Holzmann I, Agostini I, DeMatteo K, Areta JI, Merino ML, Di Bitetti MS
(2015) Using species distribution modeling to assess factors that
determine the distribution of two parapatric howlers (Alouatta spp.) in
South America. International Journal of Primatology, 36 , 18-32.
Horikawa Y (1931) A Monograph of the Mammals of Formosa. Zoological
Society of Formosa. Zoological Society of Formosa , 121 pp.
Hwang MH, Garshelis DL, Wu, YH, Wang Y (2010) Home ranges of Asiatic
black bears in the Central Mountains of Taiwan: Gauging whether a
reserve is big enough. Ursus, 21 (1), 81-96.
Ian C (1979) An evaluation of the changes of bird and mammal populations
after 6 years of hunting ban enforcement in Taiwan. Environmental
Research Center. Taitung: Tung-Hai University Press .
Ito H, Inoue-Murayama M (2019) The Tsushima leopard cat exhibits
extremely low genetic diversity compared with the Korean Amur leopard
cat: Implications for conservation. PeerJ, 7 , e7297.
Izawa M, Doi T, Nakanishi N, Teranishi A (2009) Ecology and conservation
of two endangered subspecies of the leopard cat (Prionailurus
bengalensis) on Japanese islands. Biological Conservation,
142 (9), 1884-1890.
Janzen DH (1967) Why mountain passes are higher in the tropics.The American Naturalist, 101 (919), 233-249.
John FAS, Mai CH, Pei KJC (2015) Evaluating deterrents of illegal
behaviour in conservation: carnivore killing in rural Taiwan.Biological Conservation, 189 , 86-94.
Johnson KP, Adler FR, Cherry JL (2000) Genetic and phylogenetic
consequences of island biogeography. Evolution, 54 (2), 387-396.
Johnson MT, Munshi-South J (2017) Evolution of life in urban
environments. Science, 358 (6363), eaam8327.
Jombart T (2008). adegenet: a R package for the multivariate analysis of
genetic markers. Bioinformatics, 24 (11), 1403-1405.
Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of
principal components: a new method for the analysis of genetically
structured populations. BMC genetics, 11 (1), 1-15.
Jombart T, Devillard S, Dufour AB, Pontier D (2008) Revealing cryptic
spatial patterns in genetic variability by a new multivariate method.Heredity, 101 (1), 92-103.
Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer
program CERVUS accommodates genotyping error increases success in
paternity assignment. Molecular Ecology, 16 (5), 1099-1106.
Karczmarski L, Huang SL, Wong WH, Chang WL, Chan SC, Keith M (2017)
Distribution of a coastal delphinid under the impact of long-term
habitat loss: Indo-Pacific humpback dolphins off Taiwan’s west coast.Estuaries and Coasts, 40 , 594-603.
Kerr R (1792) The animal kingdom, or zoological system, of the
celebrated Sir Charles Linnaeus; class I: Mammalia. Murray and R.
Faulder London, 400 .
Kierepka E, Latch E (2015) Performance of partial statistics in
individual‐based landscape genetics. Molecular Ecology Resources,
15 (3), 512-525.
Kimmig SE, Beninde J, Brandt M et al. (2020) Beyond the
landscape: Resistance modelling infers physical and behavioural gene
flow barriers to a mobile carnivore across a metropolitan area.Molecular Ecology, 29 (3), 466-484.
Ko BJ, An J, Eo SH (2022) Korean Leopard Cat (Prionailurus bengalensis)
population with low genetic diversity is distinct from Southeast Asian
populations. Global Ecology and Conservation, 38 , e02188.
Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015)
Clumpak: a program for identifying clustering modes and packaging
population structure inferences across K. Molecular Ecology
Resources, 15 (5), 1179-1191.
Kuehn R, Hindenlang KE, Holzgang O, Senn J, Stoeckle B, Sperisen C
(2007) Genetic effect of transportation infrastructure on roe deer
populations (Capreolus capreolus). Journal of heredity, 98 (1),
13-22.
Lande R (1988) Genetics and demography in biological conservation.Science, 241 (4872), 1455-1460.
Landguth EL, Cushman SA, Schwartz MK, McKelvey KS, Murphy M, Luikart G
(2010) Quantifying the lag time to detect barriers in landscape
genetics. Molecular Ecology, 19 (19), 4179-4191.
Landguth EL, Fedy BC, Oyler-McCance SJ et al. (2012) Effects of
sample size, number of markers, and allelic richness on the detection of
spatial genetic pattern. Molecular Ecology Resources, 12 (2),
276-284.
Larroque J, Ruette S, Vandel JM, Devillard S (2016) Divergent landscape
effects on genetic differentiation in two populations of the European
pine marten (Martes martes). Landscape Ecology, 31 , 517-531.
Laundré JW, Hernández L, Altendorf KB (2001) Wolves, elk, and bison:
reestablishing the” landscape of fear” in Yellowstone National Park,
USA. Canadian Journal of Zoology, 79 (8), 1401-1409.
Lavretsky P, McInerney NR, Mohl JE et al. (2020) Assessing
changes in genomic divergence following a century of human‐mediated
secondary contact among wild and captive‐bred ducks. Molecular
Ecology, 29 (3), 578-595.
LeDee OE, Handler SD, Hoving CL, Swanston CW, Zuckerberg B (2021).
Preparing wildlife for climate change: How far have we come? The
Journal of Wildlife Management, 85 (1), 7-16.
Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype
network construction. Methods in Ecology and Evolution, 6 (9),
1110-1116.
Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics:
combining landscape ecology and population genetics. Trends in
ecology & evolution, 18 (4), 189-197.
McCullough D (1974) Status of Larger Mammals in Taiwan: A Report to
World Wildlife Fund, Washington, DC & Tourism Bureau, Ministry of
Communications, Taiwan. Tourism Bureau, Taipei .
McLachlan JS, Hellmann JJ, Schwartz MW (2007) A framework for debate of
assisted migration in an era of climate change. Conservation
biology, 21 (2), 297-302.
McRae BH (2006) Isolation by resistance. Evolution, 60 (8),
1551-1561.
Menotti-Raymond M, David VA, Lyons LA, et al. (1999) A genetic
linkage map of microsatellites in the domestic cat (Felis catus).Genomics, 57 (1), 9-23.
Monteiro WP, Veiga JC, Silva AR et al. (2019) Everything you
always wanted to know about gene flow in tropical landscapes (but were
afraid to ask). PeerJ, 7 , e6446.
Montgelard C, Zenboudji S, Ferchaud AL, Arnal V, van Vuuren BJ (2014)
Landscape genetics in mammals. Mammalia, 78 (2), 139-157.
Moritz C, Patton JL, Conroy CJ, Parra JL, White GC, Beissinger SR (2008)
Impact of a century of climate change on small-mammal communities in
Yosemite National Park, USA. Science, 322 (5899), 261-264.
Munshi-South J (2012) Urban landscape genetics: canopy cover predicts
gene flow between white‐footed mouse (Peromyscus leucopus) populations
in New York City. Molecular Ecology, 21 (6), 1360-1378.
Naimi B, Araújo MB (2016) sdm: a reproducible and extensible R platform
for species distribution modelling. Ecography, 39 (4), 368-375.
Nikolic N, Chevalet C (2014) Detecting past changes of effective
population size. Evolutionary applications, 7 (6), 663-681.
Oksanen J, Blanchet FG, Kindt R et al. (2013). Package ‘vegan’.Community ecology package, version, 2 (9), 1-295.
Oyler-McCance SJ, Fedy BC, Landguth EL (2013) Sample design effects in
landscape genetics. Conservation Genetics, 14 , 275-285.
Pace ML, Cole JJ, Carpenter SR, Kitchell JF (1999) Trophic cascades
revealed in diverse ecosystems. Trends in ecology & evolution,
14 (12), 483-488.
Patel RP, Wutke S, Lenz D et al. (2017) Genetic structure and
phylogeography of the leopard cat (Prionailurus bengalensis) inferred
from mitochondrial genomes. Journal of heredity, 108 (4), 349-360.
Pei J (2008) Present status and conservation of small carnivores at low
elevation mountains in Shinchu County and Miaoli County (3/3). (No
Title) .
Pérez‐Espona S, McLeod JE, Franks N (2012) Landscape genetics of a top
neotropical predator. Molecular Ecology, 21 (24), 5969-5985.
Perry WL, Feder JL, Dwyer G, Lodge DM (2001) Hybrid zone dynamics and
species replacement between Orconectes crayfishes in a northern
Wisconsin lake. Evolution, 55 (6), 1153-1166.
Peterman WE (2018) ResistanceGA: An R package for the optimization of
resistance surfaces using genetic algorithms. Methods in Ecology
and Evolution, 9 (6), 1638-1647.
Peterman WE, Winiarski KJ, Moore CE, Carvalho CdS, Gilbert, A. L., &
Spear, S. F. (2019). A comparison of popular approaches to optimize
landscape resistance surfaces. Landscape Ecology, 34 , 2197-2208.
Petkova D, Novembre J, Stephens M (2016) Visualizing spatial population
structure with estimated effective migration surfaces. Nature
genetics, 48 (1), 94-100.
Petružela J, Šumbera R, Aghová T et al. (2018) Spiny mice of the
Zambezian bioregion-phylogeny, biogeography and ecological
differentiation within the Acomys spinosissimus complex. Mammalian
Biology, 91 , 79-90.
R Core Team, R. (2013). R: A language and environment for statistical
computing.
Rajaratnam R, Sunquist M, Rajaratnam L, Ambu L (2007) Diet and habitat
selection of the leopard cat (Prionailurus bengalensis borneoensis) in
an agricultural landscape in Sabah, Malaysian Borneo. Journal of
tropical ecology, 23 (2), 209-217.
Rheindt FE, Edwards SV (2011) Genetic introgression: an integral but
neglected component of speciation in birds. The Auk, 128 (4),
620-632.
Robinson SJ, Samuel MD, Lopez DL, Shelton P (2012) The walk is never
random: subtle landscape effects shape gene flow in a continuous
white‐tailed deer population in the Midwestern United States.Molecular Ecology, 21 (17), 4190-4205.
Ross J, Brodie J, Cheyne S et al. (2015) Prionailurus bengalensis. The
IUCN Red List of Threatened Species 2015. In.
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC et al. (2017). DnaSP
6: DNA sequence polymorphism analysis of large data sets.Molecular biology and evolution, 34 (12), 3299-3302.
Sattar Q, Maqbool M, Ehsan R, Akhtar S (2021) Review on climate change
and its effect on wildlife and ecosystem. Open Journal of
Environmental Biology, 6 (1), 008-014.
Segelbacher G, Cushman SA, Epperson BK et al. (2010) Applications
of landscape genetics in conservation biology: concepts and challenges.Conservation Genetics, 11 , 375-385.
Shepard EL, Wilson RP, Rees WG, Grundy E, Lambertucci SA, Vosper SB
(2013) Energy landscapes shape animal movement ecology. The
American Naturalist, 182 (3), 298-312.
Shirk A, Landguth E, Cushman S (2017) A comparison of individual‐based
genetic distance metrics for landscape genetics. Molecular Ecology
Resources, 17 (6), 1308-1317.
Shirk AJ, Landguth EL, Cushman SA (2018) A comparison of regression
methods for model selection in individual‐based landscape genetic
analysis. Molecular Ecology Resources, 18 (1), 55-67.
Shochat E, Lerman SB, Anderies JM, Warren PS, Faeth SH, Nilon CH (2010)
Invasion, competition, and biodiversity loss in urban ecosystems.BioScience, 60 (3), 199-208.
Short Bull R, Cushman S, Mace R et al. (2011) Why replication is
important in landscape genetics: American black bear in the Rocky
Mountains. Molecular Ecology, 20 (6), 1092-1107.
Slatkin M (1987) Gene flow and the geographic structure of natural
populations. Science, 236 (4803), 787-792.
Sunquist M, Sunquist F (2017) Wild cats of the world : University
of chicago press.
Sunquist M, Sunquist F, Wilson D, Mittermeier R (2009) A Handbook of the
Mammals of the World, Volume 1: Carnivores. Lynx Editions,
Barcelona, Spain .
Tamada T, Siriaroonrat B, Subramaniam V et al. (2008) Molecular
diversity and phylogeography of the Asian leopard cat, Felis
bengalensis, inferred from mitochondrial and Y-chromosomal DNA
sequences. Zoological science, 25 (2), 154-163.
Taylor KE, Stouffer RJ, Meehl GA (2012) An overview of CMIP5 and the
experiment design. Bulletin of the American meteorological
Society, 93 (4), 485-498.
Teng Y, Yang J, Ju LF et al. (2022) Current Genetic Structure
Analysis of Leopard Cats Reveals a Weak Disparity Trend in
Subpopulations in Beijing, China. Biology, 11 (10), 1478.
Terborgh J, Estes JA, Paquet P, Ralls K, Boyd-Heger D, Miller BJ, Noss
RF (1999) The role of top carnivores in regulating terrestrial
ecosystems. Continental conservation: scientific foundations of
regional reserve networks , 39-64.
Thatte P, Joshi A, Vaidyanathan S, Landguth E, Ramakrishnan U (2018)
Maintaining tiger connectivity and minimizing extinction into the next
century: Insights from landscape genetics and spatially-explicit
simulations. Biological Conservation, 218 , 181-191.
Toews DP, Brelsford A (2012) The biogeography of mitochondrial and
nuclear discordance in animals. Molecular Ecology, 21 (16),
3907-3930.
Tuomainen U, Candolin U (2011) Behavioural responses to human‐induced
environmental change. Biological Reviews, 86 (3), 640-657.
Turner MG (1989) Landscape ecology: the effect of pattern on process.Annual review of Ecology and Systematics, 20 (1), 171-197.
van der Meer E, Dullemont H, Wang CH et al. (2023) Fine-Scaled
Selection of Resting and Hunting Habitat by Leopard Cats (Prionailurus
bengalensis) in a Rural Human-Dominated Landscape in Taiwan.Animals, 13 (2), 234.
van Etten J (2017) R package gdistance: distances and routes on
geographical grids. Journal of Statistical Software, 76 , 1-21.
van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004)
MICRO‐CHECKER: software for identifying and correcting genotyping errors
in microsatellite data. Molecular ecology notes, 4 (3), 535-538.
Velo-Antón G, Lourenço A, Galán P, Nicieza A, Tarroso P (2021) Landscape
resistance constrains hybridization across contact zones in a
reproductively and morphologically polymorphic salamander.Scientific Reports, 11 (1), 9259.
Wang IJ (2011) Choosing appropriate genetic markers and analytical
methods for testing landscape genetic hypotheses. In: Wiley Online
Library.
Warren MJ (2013) Cougar genetic variation and gene flow in a
heterogeneous landscape.
Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates
using multilocus genotypes. Genetics, 163 (3), 1177-1191.
Wilson RP, Quintana F, Hobson VJ (2012) Construction of energy
landscapes can clarify the movement and distribution of foraging
animals. Proceedings of the Royal Society B: Biological Sciences,
279 (1730), 975-980.
Wong BB, Candolin U (2015) Behavioral responses to changing
environments. Behavioral Ecology, 26 (3), 665-673.
Wood JR, Alcover JA, Blackburn TM et al. (2017) Island
extinctions: processes, patterns, and potential for ecosystem
restoration. Environmental conservation, 44 (4), 348-358.
Wu TM (2004) Economic history of Taiwan: a survey. Australian
Economic History Review, 44 (3), 294-306.
Yumnam B, Jhala YV, Qureshi Q et al. (2014) Prioritizing tiger
conservation through landscape genetics and habitat linkages. PLoS
One, 9 (11), e111207.
Zeller KA, McGarigal K, Whiteley AR (2012) Estimating landscape
resistance to movement: a review. Landscape Ecology, 27 , 777-797.