Abstract
Context
In natural populations, gene flow often represents a key factor in determining and maintaining genetic diversity. In a worldwide context of habitat fragmentation, assessing the relative contribution of landscape features to gene flow thus appears crucial for sustainable management of species.
Objective
We addressed this issue in Mediterranean mouflon (Ovis gmelini musimon × Ovis sp.) by combining previous knowledge on behavioral ecology with landscape genetics. We also assessed how sex-specific behavioral differences translated in term of functional connectivity in both sexes.
Methods
We relied on 239 individuals genotyped at 16 microsatellite markers. We applied a model optimization approach in a causal modeling framework of landscape genetics to test for the effects on gene flow of habitat types and linear landscape features previously identified as important for movements and habitat selection in both sexes. Five resistance values were alternately assigned to these landscape characteristics leading to a comprehensive set of resistance surfaces.
Results
Isolation by resistance shaped female gene flow, supporting the central role of linear landscape features as behavioral barriers for animal movements. Conversely, no isolation by resistance was detected in males. Although a lack of statistical power cannot be discarded to explain this result, it tended to confirm that males are less influenced by landscape structures during the mating period.
Conclusions
Combining previous knowledge on behavioral ecology with results from landscape genetics was decisive in assessing functional landscape connectivity in both sexes. These results highlighted the need to perform sex-specific studies for management and conservation of dimorphic species.
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Data availability
Microsatellite and spatial data sets will be available from the Dryad Digital Repository.
References
Abrahms B, Sawyer SC, Jordan NR, McNutt JW, Wilson AM, Brashares JS (2017) Does wildlife resource selection accurately inform corridor conservation? J Appl Ecol 54:412–422
Altizer S, Nunn CL, Thrall PH, Gittleman JL, Antonovics J, Cunningham AA, Dobson AP, Ezenwa V, Jones KE, Pedersen AB, Poss M, Pulliam JRC (2003) Social organization and parasite risk in mammals: integrating theory and empirical studies. Annu Rev Ecol Evol Syst 34:517–547
Baguette M, Van Dyck H (2007) Landscape connectivity and animal behavior: functional grain as a key determinant for dispersal. Landscape Ecol 22:1117–1129
Balkenhol N, Cushman SA, Storfer AT, Waits LP (2016) Landscape genetics: concepts, methods, applications. Wiley-Blackwell, West Sussex, UK
Barros T, Cushman SA, Carvalho J, Fonseca C (2016) Mediterranean scrubland and elevation drive gene flow of a Mediterranean carnivore, the Egyptian mongoose Herpestes ichneumon (Herpestidae). Biol J Linn Soc 120:195–209
Bartzke GS, May R, Solberg EJ, Rolandsen CM, Røskaft E (2015) Differential barrier and corridor effects of power lines, roads and rivers on moose (Alces alces) movements. Ecosphere 6:art67
Baudière A (1970) Recherches phytogéographiques sur la bordure méridionale du Massif Central français (Les Monts de l’Espinouse). Thèse de doctorat, Université de Montpellier, Montpellier, France
Benoist S, Garel M, Cugnasse JM, Blanchard P (2013) Human disturbances, habitat characteristics and social environment generate sex-specific responses in vigilance of Mediterranean mouflon. PLoS ONE 8:e82960
Bertolino S, Di Montezemolo NC, Bassano B (2009) Food-niche relationships within a guild of alpine ungulates including an introduced species. J Zool 277:63–69
Beyer HL, Gurarie E, Börger L, Panzacchi M, Basille M, Herfindal I, Van Moorter B, R. Lele S, Matthiopoulos J (2016) “You shall not pass!”: quantifying barrier permeability and proximity avoidance by animals. J Anim Ecol 85:43–53
Blazquez-Cabrera S, Gastón A, Beier P, Garrote G, Simón MÁ, Saura S (2016) Influence of separating home range and dispersal movements on characterizing corridors and effective distances. Landscape Ecol 31:2355–2366
Bon R, Campan R (1989) Social tendencies of the Corsican Mouflon Ovis ammon musimon in the Caroux-Espinouse massif (South of France). Behav Process 19:57–78
Bon R, Dardaillon M, Estevez I (1993) Mating and lambing periods as related to age of female mouflon. J Mammal 74:752–757
Bon R, Gonzalez G, Bosch MD, Cugnasse JM (1992) Ram rut-involvement in a hunted population of mouflons. Acta Theriol 37:63–71
Bon R, Recarte JM, Gonzalez G, Cugnasse JM (1995) Courtship and behavioral maturation of male mouflons. Acta Theriol 40:283–294
Bourgoin G, Marchand P, Hewison AJM, Ruckstuhl KE, Garel M (2018) Social behaviour as a predominant driver of sexual, age-dependent and reproductive segregation in Mediterranean mouflon. Anim Behav 136:87–100
Breyne P, Mergeay J, Casaer J (2014) Roe deer population structure in a highly fragmented landscape. Eur J Wildl Res 60:909–917
Bruggeman JE, Garrott RA, Bjornlie D, White PJ, Watson FGR, Borkowski JJ (2006) Temporal variability in winter travel patterns of Yellowstone bison: the effects of road grooming. Ecol Appl 16:1539–1554
Bruggeman JE, Garrott RA, White PJ, Watson FGR, Wallen R (2007) Covariates affecting spatial variability in bison travel behavior in Yellowstone National Park. Ecol Appl 17:1411–1423
Bull RAS, Cushman SA, Mace R, Chilton T, Kendall KC (2011) Why replication is important in landscape genetics: American black bear in the Rocky Mountains. Mol Ecol 20:1092–1107
Cazau M, Garel M, Maillard D (2011) Responses of heather moorland and Mediterranean mouflon foraging to prescribed-burning and cutting. J Wildl Manage 75:967–972
Chapuis JL, Boussès P, Barnaud G (1994) Alien mammals, impact and management in the French subantarctic islands. Biol Conserv 67:97–104
Chen HL, Koprowski JL (2016) Barrier effects of roads on an endangered forest obligate: influences of traffic, road edges, and gaps. Biol Conserv 199:33–40
Ciuti S, Northrup JM, Muhly TB, Simi S, Musiani M, Pitt JA, Boyce MS (2012) Effects of humans on behaviour of wildlife exceed those of natural predators in a landscape of fear. PLoS ONE 7:e50611
Ciuti S, Pipia A, Grignolio S, Ghiandai F, Apollonio M (2009) Space use, habitat selection and activity patterns of female sardinian mouflon (Ovis orientalis musimon) during the lambing season. Eur J Wildl Res 55:589–595
Clutton-Brock TH, Lukas D (2012) The evolution of social philopatry and dispersal in female mammals. Mol Ecol 21:472–492
Coltman DW, Festa-Bianchet M, Jorgenson JT, Strobeck C (2002) Age-dependent sexual selection in bighorn rams. Proc R Soc B Biol Sci 269:165–172
Conner MM, Miller MW (2004) Movement patterns and spatial epidemiology of a prion disease in mule deer population units. Ecol Appl 14:1870–1881
Coulon A, Cosson JF, Angibault JM, Cargnelutti B, Galan M, Morellet N, Petit E, Aulagnier S, Hewisson AJM (2004) Landscape connectivity influences gene flow in a roe deer population inhabiting a fragmented landscape: an individual–based approach. Mol Ecol 13:2841–2850
Coulson T, Albon S, Pilkington J, Clutton-Brock T (1999) Small scale spatial dynamics in fluctuating ungulate population. J Anim Ecol 68:658–671
Cozzi G, Broekhuis F, Mcnutt JW, Schmid B (2013) Comparison of the effects of artificial and natural barriers on large African carnivores: implications for interspecific relationships and connectivity. J Anim Ecol 82:707–715
Cransac N, Gerard JF, Maublanc ML, Pépin D (1998) An example of segregation between age and sex classes only weakly related to habitat use in mouflon sheep (Ovis gmelini). J Zool 244:371–378
Cransac N, Valet G, Cugnasse JM, Rech J (1997) Seasonal diet of mouflon (Ovis gmelini): comparison of population sub-units and sex-age classes. La Terre la Vie 52:21–36
Creech TG, Epps CW, Landguth EL, Wehausen JD, Crowhurst RS, Holton B, Monello RJ (2017) Simulating the spread of selection-driven genotypes using landscape resistance models for desert bighorn sheep. PLoS ONE 12:e0176960
Crooks KR, Sanjayan M (2006) Connectivity conservation: maintaining connections for nature. In: Crooks KR, Sanjayan M (eds) Connectivity conservation. Cambridge University Press, Cambridge, pp 1–28
Cugnasse JM (1990) Inventaire faunistique du massif du Caroux et des monts de l’Espinouse (Hérault):(mammifères, oiseaux, reptiles et batraciens). Office national de la chasse, Station d’étude sur la faune des milieux méditerranéens, Paris, France
Cushman SA, McKelvey KS, Hayden J, Schwartz M (2006) Gene flow in complex landscapes: testing multiple hypotheses with causal modeling. Am Nat 168:486–499
Cushman SA, Wasserman TN, Landguth EL, Shirk AJ (2013) Re-evaluating causal modeling with mantel tests in landscape genetics. Diversity 5:51–72
D’Amico M, Périquet S, Román J, Revilla E (2016) Road avoidance responses determine the impact of heterogeneous road networks at a regional scale. J Appl Ecol 53:181–190
Dubois M, Bon R, Cransac N, Maublanc ML (1994) Dispersal patterns of Corsican mouflon ewes: importance of age and proximate influences. Appl Anim Behav Sci 42:29–40
Dubois M, Gerard J, Maublanc ML (1992) Seasonal movements of females Corsican mouflon (Ovis ammon) in a Mediterranean mountain range, southern France. Behav Process 26:155–166
Dubois M, Khazraïe K, Guilhem C, Maublanc ML, Le Pendu Y (1996) Philopatry in mouflon rams during the rutting season: psycho-ethological determinism and functional consequences. Behav Process 35:93–100
Dubois M, Quenette P-Y, Bideau E (1993) Seasonal range use by European mouflon rams in medium altitude mountains. Acta Theriol 38:185–198
Dupuis J, Badia J, Maublanc ML, Bon R (2002) Survival and spatial fidelity of mouflon (Ovis gmelini): a bayesian analysis of an age-dependent capture-recapture model. J Agric Biol Environ Stat 7:277–298
Dussault C, Ouellet J, Courtois R, Huot J, Breton L, Jolicoeur H (2005) Linking moose habitat selection to limiting factors. Ecography 28:619–628
Ehrlich PR (1961) Intrinsic barriers to dispersal in checkerspot butterfly. Science 134:108–109
Epps CW, McCullough DR, Wehausen JD, Bleich VC, Rechel JL (2004) Effects of climate change on population persistence of desert-dwelling mountain sheep in California. Conserv Biol 18:102–113
Epps CW, Palsbøll PJ, Wehausen JD, Roderick GK, McCullough DR (2006) Elevation and connectivity define genetic refugia for mountain sheep as climate warms. Mol Ecol 15:4295–4302
Epps CW, Palsboll 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. Ecol Lett 8:1029–1038
Epps CW, Wehausen JD, Bleich VC, Torres SG, Brashares JS (2007) Optimizing dispersal and corridor models using landscape genetics. J Appl Ecol 44:714–724
Etherington TR, Penelope Holland E (2013) Least-cost path length versus accumulated-cost as connectivity measures. Landscape Ecol 28:1223–1229
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515
Festa-Bianchet M (1988) Seasonal range selection in bighorn sheep: conflicts between forage quality, forage quantity, and predator avoidance. Oecologia 75:580–586
Festa-Bianchet M (1991) The social system of bighorn sheep: grouping patterns, kinship and female dominance rank. Anim Behav 42:71–82
Festa-Bianchet M (2012) The cost of trying: weak interspecific correlations among life-history components in male ungulates. Can J Zool 90:1072–1085
Focardi S, Raganella Pelliccioni E, Petrucco R, Toso S (2002) Spatial patterns and density dependence in the dynamics of a roe deer (Capreolus capreolus) population in central Italy. Oecologia 130:411–419
Frankham R, Ballou JD, Briscoe DA (2004) A primer of conservation genetics. Cambridge University Press, New York
Frantz AC, Bertouille S, Eloy MC, Licoppe A, Chaumont F, Flamand MC (2012) Comparative landscape genetic analyses show a Belgian motorway to be a gene flow barrier for red deer (Cervus elaphus), but not wild boars (Sus scrofa). Mol Ecol 21:3445–3457
Frantz AC, Pope LC, Etherington TR, Wilson GJ, Burke T (2010) Using isolation-by-distance-based approaches to assess the barrier effect of linear landscape elements on badger (Meles meles) dispersal. Mol Ecol 19:1663–1674
Garel M, Cugnasse JM, Loison A, Gaillard JM, Vuiton C, Maillard D (2005) Monitoring the abundance of mouflon in South France. Eur J Wildl Res 51:69–76
Garel M, Cugnasse JM, Maillard D, Gaillard JM, Hewison AJM, Dubray D (2007) Selective harvesting and habitat loss produce long-term life history changes in a mouflon population. Ecol Appl 17:1607–1618
Geist V (1971) Mountain sheep: a study in behavior and evolution. University of Chicago Press, Chicago, Illinois
Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19
Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162
Gross JE, Singer FJ, Moses ME (2000) Effects of disease, dispersal and area on bighorn sheep restoration. Restor Ecol 8:25–37
Gubili C, Mariani S, Weckworth BV, Galpern P, McDevitt AD, Hebblewhite M, Nickel B, Musiani M (2017) Environmental and anthropogenic drivers of connectivity patterns: a basis for prioritizing conservation efforts for threatened populations. Evol Appl 10:199–211
Hamel S, Gaillard JM, Yoccoz NG, Albon S, Côté SD, Craine JM, Festa-Bianchet M, Garel M, Lee P, Moss C, Nussey DH, Pelletier F, Stien A, Tveraa T (2016) Cohort variation in individual body mass dissipates with age in large herbivores. Ecol Monogr 86:517–543
Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620
Harris RB, Pletscher DH (2002) Incentives toward conservation of argali Ovis ammon: a case study of trophy hunting in Western China. Oryx 36:373–381
Harris RJ, Reed JM (2002) Behavioral barriers to non-migratory movements of birds. Ann Zool Fenn 39:275–290
Hepenstrick D, Thiel D, Holderegger R, Gugerli F (2012) Genetic discontinuities in roe deer (Capreolus capreolus) coincide with fenced transportation infrastructure. Basic Appl Ecol 13:631–638
Hofer D (2002) The lion’s share of the hunt: Trophy hunting and conservation: A review of the legal eurasian tourist hunting market and trophy trade under cites. Technical report, TRAFFIC Europe, Brussels, Belgium
Hogg JT (1984) Mating in bighorn sheep: multiple creative male strategies. Science 225:526–529
Hogg JT (1987) Intrasexual competition and mate choice in rocky mountain bighorn sheep. Ethology 75:119–144
Hogg JT, Forbes SH (1997) Mating in bighorn sheep: frequent male reproduction via a high-risk “unconventional” tactic. Behav Ecol Sociobiol 41:33–48
Imong I, Robbins MM, Mundry R, Bergl R, Kühl HS (2014) Informing conservation management about structural versus functional connectivity: a case-study of Cross River gorillas. Am J Primatol 76:978–988
Jarman P (1983) Mating system and sexual dimorphism in large, terrestrial, mammalian herbivores. Biol Rev 58:485–520
Jarnemo A (2011) Male red deer (Cervus elaphus) dispersal during the breeding season. J Ethol 29:329–336
Karns GR, Lancia RA, DePerno CS, Conner MC (2011) Investigation of adult male white-tailed deer excursions outside their home range. Southeast Nat 10:39–52
Keeley ATH, Beier P, Keeley BW, Fagan ME (2017) Habitat suitability is a poor proxy for landscape connectivity during dispersal and mating movements. Landsc Urban Plan 161:90–102
King R, Brooks SP (2003) Survival and spatial fidelity of mouflons: the effect of location, age, and sex. J Agric Biol Environ Stat 8:486–513
Koen EL, Garroway CJ, Wilson PJ, Bowman J (2010) The effect of map boundary on estimates of landscape resistance to animal movement. PLoS ONE 5:1–8
Kuehn R, Hindenlang KE, Holzgang O, Senn J, Stoeckle B, Sperisen C (2007) Genetic effect of transportation infrastructure on roe deer populations (Capreolus capreolus). J Hered 98:13–22
Lande R (1998) Anthropogenic, ecological and genetic factors in extinction and conservation. Res Popul Ecol 40:259–269
Landguth EL, Cushman SA, Schwartz MK, McKelvey KS, Murhpy M, Luikart G (2010) Quantifying the lag time to detect barriers in landscape genetics. Mol Ecol 19:4179–4191
Larroque J (2015) Same looks, different ecology: ecological and genetic insights on two syntopic mustelids species, the European Pine marten (Martes martes) and the Stone marten (Martes foina). Thèse de doctorat, Université de Lyon, Lyon, France
Larroque J, Ruette S, Vandel J-M, Devillard S (2016a) Divergent landscape effects on genetic differentiation in two populations of the European pine marten (Martes martes). Landscape Ecol 31:517–531
Larroque J, Ruette S, Vandel JM, Queney G, Devillard S (2016b) Age and sex-dependent effects of landscape cover and trapping on the spatial genetic structure of the stone marten (Martes foina). Conserv Genet 17:1293–1306
Laundré JW, Hernández L, Altendorf KB (2001) Wolves, elk, and bison: reestablishing the “landscape of fear” in Yellowstone National Park, U.S.A. Can J Zool 79:1401–1409
Laurian C, Dussault C, Ouellet J-P, Courtois R, Poulin M, Breton L (2008) Behavior of moose relative to a road network. J Wildl Manag 72:1550–1557
Le Pendu Y, Maublanc ML, Briedermann L, Dubois M (1996) Spatial structure and activity in groups of Mediterranean mouflon (Ovis gmelini). A comparative study. Appl Anim Behav Sci 46:201–216
Legendre P (1993) Spatial autocorrelation: trouble or new paradigm? Ecology 74:1659–1673
Legendre P, Fortin MJ, Borcard D (2015) Should the Mantel test be used in spatial analysis? Methods Ecol Evol 6:1239–1247
Legendre P, Troussellier M (1988) Aquatic heterotrophic bacteria: modeling in the presence of spatial autocorrelation. Limnol Oceanogr 33:1055–1067
Long ES, Diefenbach DR, Wallingford BD, Rosenberry CS (2010) Influence of roads, rivers, and mountains on natal dispersal of white-tailed deer. J Wildl Manag 74:1242–1249
Lowe WH, Allendorf FW (2010) What can genetics tell us about population connectivity? Mol Ecol 19:3038–3051
Mabille G, Dussault C, Ouellet JP, Laurian C (2012) Linking trade-offs in habitat selection with the occurrence of functional responses for moose living in two nearby study areas. Oecologia 170:965–977
Maiorano L, Boitani L, Chiaverini L, Ciucci P (2017) Uncertainties in the identification of potential dispersal corridors: the importance of behaviour, sex, and algorithm. Basic Appl Ecol 21:66–75
Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197
Marchand P (2013) Déterminants spatio-temporels de la sélection de l’habitat chez le mouflon méditerranéen Ovis gmelini musimon × Ovis sp. Thèse de doctorat, Université de Grenoble, Grenoble, France
Marchand P, Freycon P, Herbaux J, Game Y, Toïgo C, Gilot-fromont E, Rossi S, Hars J (2017a) Sociospatial structure explains marked variation in brucellosis seroprevalence in an Alpine ibex population. Sci Rep 7:1–12
Marchand P, Garel M, Bourgoin G, Dubray D, Maillard D, Loison A (2014a) Impacts of tourism and hunting on a large herbivore’s spatio-temporal behavior in and around a French protected area. Biol Conserv 177:1–11
Marchand P, Garel M, Bourgoin G, Dubray D, Maillard D, Loison A (2015) Coupling scale-specific habitat selection and activity reveals sex-specific food/cover trade-offs in a large herbivore. Anim Behav 102:169–187
Marchand P, Garel M, Bourgoin G, Duparc A, Dubray D, Maillard D, Loison A (2017b) Combining familiarity and landscape features helps break down the barriers between movements and home ranges in a non-territorial large herbivore. J Anim Ecol 86:371–383
Marchand P, Garel M, Bourgoin G, Michel P, Maillard D, Loison A (2014b) Habitat-related variation in carcass mass of a large herbivore revealed by combining hunting and GPS data. J Wildl Manag 78:657–670
Marchand P, Redjadj C, Garel M, Cugnasse JM, Maillard D, Loison A (2013) Are mouflon Ovis gmelini musimon really grazers? A review of variation in diet composition. Mamm Rev 43:275–291
Martinetto K, Cugnasse J, Gilbert Y (1998) La cohabitation du mouflon Méditerranéen (Ovis gmelini musimon x Ovis sp.) et des touristes dans le massif du Caroux-Espinouse (Hérault). Gibier Faune Sauvage 15:905–919
Martins AG, Netto NT, Aulagnier S, Borges A, Dubois M, Vicente L, Gerard J-F, Maublanc ML (2002) Population subdivision among mouflon sheep (Ovis gmelini) ewes and ranging behaviour of rams during the rut. J Zool 258:27–37
Mateo-Sánchez MC, Balkenhol N, Cushman SA, Pérez T, Domínguez A, Saura S (2015) A comparative framework to infer landscape effects on population genetic structure: are habitat suitability models effective in explaining gene flow? Landscape Ecol 30:1405–1420
McRae BH (2006) Isolation by resistance. Evolution 60:1551–1561
Moilanen A, Hanski I (1998) Metapopulation dynamics: effects of habitat quality and landscape structure. Ecology 79:2503–2515
Moran EV, Hartig F, Bell DM (2016) Intraspecific trait variation across scales: implications for understanding global change responses. Glob Chang Biol 22:137–150
Nathan R, Getz WM, Revilla E, Holyoak M, Kadmon R, Saltz D, Smouse PE (2008) A movement ecology paradigm for unifying organismal movement research. PNAS 105:19052–19059
Noble CW, Bono JM, Pigage HK, Hale DW, Pigage JC (2016) Fine-scale genetic structure in female mule deer (Odocoileus hemionus). West North American Nat 76:417–426
Nogales M, Rodriguez-Luengo JL, Marrero P (2006) Ecological effects and distribution of invasive non-native on the Canary Islands. Mamm Rev 36:49–65
Nussey DH, Coltman DW, Coulson T, Kruuk LEB, Donald A, Morris SJ, Clutton-Brock TH, Pemberton J (2005) Rapidly declining fine-scale spatial genetic structure in female red deer. Mol Ecol 14:3395–3405
Olah G, Smith AL, Asner GP, Brightsmith DJ, Heinsohn RG, Peakall R (2017) Exploring dispersal barriers using landscape genetic resistance modelling in scarlet macaws of the Peruvian Amazon. Landscape Ecol 32:445–456
Panzacchi M, Van Moorter B, Strand O, Saerens M, Kivimäki I, St. Clair CC, Herfindal I, Boitani L (2016) Predicting the continuum between corridors and barriers to animal movements using Step Selection Functions and Randomized Shortest Paths. J Anim Ecol 85:32–42
Parks LC, Wallin DO, Cushman SA, McRae BH (2015) Landscape-level analysis of mountain goat population connectivity in Washington and southern British Columbia. Conserv Genet 16:1195–1207
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
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
Pelletier F, Mainguy J, Côté SD (2009) Rut-induced hypophagia in male bighorn sheep and mountain goats: foraging under time budget constraints. Ethology 115:141–151
Pépin D, Morellet N, Goulard M (2009) Seasonal and daily walking activity patterns of free-ranging adult red deer (Cervus elaphus) at the individual level. Eur J Wildl Res 55:479–486
Perez-Espona S, Perez-Barberia FJ, Mcleod JE, Jiggins CD, Gordon IJ, Pemberton JM (2008) Landscape features affect gene flow of Scottish Highland red deer (Cervus elaphus). Mol Ecol 17:981–996
Pettorelli N, Dray S, Gaillard JM, Chessel D, Duncan P, Illius A, Guillon N, Klein F, Van Laere G (2003) Spatial variation in springtime food resources influences the winter body mass of roe deer fawns. Oecologia 137:363–369
Pettorelli N, Gaillard JM, Duncan P, Ouellet JP, Van Laere G (2001) Population density and small-scale variation in habitat quality affect phenotypic quality in roe deer. Oecologia 128:400–405
Plard F, Gaillard J, Coulson T, Delorme D, Warnant C, Michallet J, Tuljapurkar S, Krishnakumar S, Bonenfant C, Lyon D, Lyon F-, De Biom L (2015) Quantifying the influence of measured and unmeasured individual differences on demography. J Anim Ecol 84:1434–1445
Podgórski T, Scandura M, Jedrzejewska B (2014) Next of kin next door—philopatry and socio-genetic population structure in wild boar. J Zool 294:190–197
Portanier E, Garel M, Devillard S, Marchand P, Andru J, Maillard D, Bourgoin G (2017) Introduction history overrides social factors in explaining genetic structure of females in Mediterranean mouflon. Ecol Evol 7:1–12
Prokopenko CM, Boyce MS, Avgar T (2017) Characterizing wildlife behavioural responses to roads using integrated step selection analysis. J Appl Ecol 54:470–479
Ray N, Lehmann A, Joly P (2002) Modeling spatial distribution of amphibian populations: a GIS approach based on habitat matrix permeability. Biodivers Conserv 11:2143–2165
Reding DM, Cushman SA, Gosselink TE, Clark WR (2013) Linking movement behavior and fine-scale genetic structure to model landscape connectivity for bobcats (Lynx rufus). Landscape Ecol 28:471–486
Richardson JL, Brady SP, Wang IJ, Spear SF (2016) Navigating the pitfalls and promise of landscape genetics. Mol Ecol 25:849–863
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. Mol Ecol 21:4190–4205
Roffler GH, Schwartz MK, Pilgrim KL, Talbot SL, Sage GK, Adams LG, Luikart G (2016) Identification of landscape features influencing gene flow: how useful are habitat selection models? Evol Appl 9:805–817
Rousset F (2000) Genetic differentiation between individuals. J Evol Biol 13:58–62
Ruckstuhl KE, Neuhaus P (2006) Sexual segregation in vertebrates - ecology of the two sexes. Cambridge University Press, Cambridge
Segelbacher G, Cushman SA, Epperson BK, Fortin MJ, Francois O, Hardy OJ, Holderegger R, Taberlet P, Waits LP, Manel S (2010) Applications of landscape genetics in conservation biology: concepts and challenges. Conserv Genet 11:375–385
Seidler RG, Long RA, Berger J, Bergen S, Beckmann JP (2014) Identifying impediments to long-distance mammal migrations. Conserv Biol 29:99–109
Shackleton, DM, IUCN/SSC Caprinae Specialist Group (1997) Wild sheep and goats and their relatives: status survey and conservation action plan for Caprinae. IUCN, Gland, Switzerland and Cambridge
Shirk AJ, Landguth EL, Cushman SA (2017) A comparison of individual-based genetic distance metrics for landscape genetics. Mol Ecol Resour 17:1308–1317
Shirk AJ, Landguth EL, Cushman SA (2018) A comparison of regression methods for model selection in individual-based landscape genetic analysis. Mol Ecol Resour 18:55–67
Shirk AJ, Wallin DO, Cushman SA, Rice CG, Warheit KI (2010) Inferring landscape effects on gene flow: a new model selection framework. Mol Ecol 19:3603–3619
Taylor PD, Fahrig L, Henein K, Merriam G (1993) Connectivity is a vital element of landscape structure. Oikos 68:571–573
Taylor P, Fahrig L, With K (2006) Landscape connectivity: a return to the basics. In: Crooks KR, Sanjayan M (eds) Connectivity conservation. Cambridge University Press, Cambridge, pp 29–43
Tronchot M (2008) Cartographie des habitats du massif du Caroux-Espinouse (Hérault) à partir de photos aeriennes de 2005. Technical report. Groupement d’Interêt Environnemental et Cynégétique du Caroux-Espinouse - Office National de la Chasse et de la Faune Sauvage, Paris, France
Unterthiner S, Ferretti F, Rossi L, Lovari S (2012) Sexual and seasonal differences of space use in Alpine chamois. Ethol Ecol Evol 24:257–274
Valdez R (2008) Ovis orientalis. The IUCN Red List of Threatened Species 2008: e.T15739A5076068
van Etten J (2017) R Package gdistance: distances and routes on geographical grids. J Stat Softw 76:1–21
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
Wasserman TN, Cushman SA, Schwartz MK, Wallin DO (2010) Spatial scaling and multi-model inference in landscape genetics: Martes americana in northern Idaho. Landscape Ecol 25:1601–1612
White KS, Gregovich DP, Barten NL, Scott R (2012) Moose population ecology and habitat use along the Juneau Access road corridor, Alaska. Final wildlife research report. ADF&G/DWC/WRR-2012-03. Alaska Department of Fish and Game, Juneau, AK. USA
Wilson RE, Farley SD, McDonough TJ, Talbot SL, Barboza PS (2015) A genetic discontinuity in moose (Alces alces) in Alaska corresponds with fenced transportation infrastructure. Conserv Genet 16:791–800
Worley K, Strobeck C, Arthur A, Carey J, Schwantje H, Veitch A, Coltman DW (2004) Population genetic structure of North American thinhorn sheep (Ovis dalli). Mol Ecol 13:2545–2556
Zeller KA, Creech TG, Millette KL, Crowhurst RS, Long RA, Wagner HH, Balkenhol N, Landguth EL (2016) Using simulations to evaluate Mantel-based methods for assessing landscape resistance to gene flow. Ecol Evol 6:4115–4128
Zeller KA, McGarigal K, Whiteley AR (2012) Estimating landscape resistance to movement: a review. Landscape Ecol 27:777–797
Zimmermann B, Nelson L, Wabakken P, Sand H, Liberg O (2014) Behavioral responses of wolves to roads: scale-dependent ambivalence. Behav Ecol 25:1353–1364
Acknowledgements
We warmly thank all the professionals from the Office National de la Chasse et de la Faune Sauvage (Service Départemental 34, Jeanne Duhayer and Christian Itty) and numerous trainees for their technical support in trapping, tagging, sampling, and monitoring VHF and GPS-collared mouflons. We would like to thank Dominique Dubray for his involvement in the deployment of GPS collars, all the technical personnel of LBBE for helping with laboratory steps of the study, and the Antagene laboratory (Limonest, France, www.antagene.com) for DNA extraction and genotyping. We would also like to thank Elodie Bonneau and Julie Andru for the first laboratory and genetic analyses, Patrick James and the James lab members for helpful comments on the first draft of the manuscript, and Denise Mirat for checking the English. We also gratefully acknowledge IN2P3 and the CC LBBE/PRABI for providing computer resources, and the bioinformatics team of LBBE for their advice on computational optimization of scripts. Finally, we thank two anonymous referees for helpful comments on the manuscript. This research project and E. Portanier’s collaboration were funded by the Office National de la Chasse et de la Faune Sauvage, Vetagro Sup and LBBE.
Funding
This study was funded by the Office National de la Chasse et de la Faune Sauvage, VetagroSup and Laboratoire de Biométrie et de Biologie Evolutive (Grant Numbers 2013/20/6171 and 2015/14/6171).
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EP, MG, PM, DM, GB and SD conceptualized and designed the research. EP, JL, MG, PM and SD conducted data analyses. All authors contributed in interpreting the results and writing the paper.
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Portanier, E., Larroque, J., Garel, M. et al. Landscape genetics matches with behavioral ecology and brings new insight on the functional connectivity in Mediterranean mouflon. Landscape Ecol 33, 1069–1085 (2018). https://doi.org/10.1007/s10980-018-0650-z
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DOI: https://doi.org/10.1007/s10980-018-0650-z