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Genetic structure of populations of the Pampean grassland mouse, Akodon azarae, in an agroecosystem under intensive management

Abstract

Agroecosystems in central Argentina are a good example of landscape modification by human activities. We used the Pampean grassland mouse (Akodon azarae) as a biological model to assess the effects of landscape fragmentation on the genetic structure of natural populations present in the region. The species is a habitat specialist that is numerically dominant in relatively stable environments, such as remnant areas of native vegetation, stream borders, roadsides and railway banks. We used seven microsatellite loci to analyze the genetic population structure and to explore if there is sex-biased dispersal during the reproductive season at a fine geographical scale. Rodents were captured seasonally in trap lines located on roadsides in an agroecosystem of central Argentina. Values of genetic differentiation among populations and temporal patterns of spatial autocorrelation revealed that the genetic populations occupy areas larger than the sampling area. Causal modeling analyses showed that unfavorable habitats (secondary roads and crop fields) were not barriers to dispersal of Akodon azarae. The high levels of gene flow and the short duration of the low population density phase, followed by a fast recovery, would contribute to the maintenance of highly polymorphic populations. As expected for A. azarae’s mating system, males were not genetically structured. However, females’ spatial genetic structure varied greatly over the year, which would be related to availability and quality of habitat, and to intrasex interactions. Our work contributes to the understanding of dispersal strategies in small mammals in anthropogenically fragmented habitats like intensively managed agroecosystems.

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References

  1. Alberto, F., 2009. MsatAllele-1.0: an R package to visualize the binning of microsatellite alleles. J. Hered. 100, 394–397, https://doi.org/10.1093/jhered/esn110.

  2. Andreo, V., Provensal, C., Scavuzzo, M., Lamfri, M., Polop, J., 2009. Environmental factors and population fluctuations of Akodon azarae (Muridae: Sigmodontinae) in central Argentina. Austral Ecol. 34, 132–142, https://doi.org/10.1111/j.1442-9993.2008.01889.x.

  3. Ávila, B., Bonatto, F., Priotto, J., Steinmann, A.R., 2016. Effects of high density on spacing behaviour and reproduction in Akodon azarae: a fencing experiment. ActaOecol. 70, 67–73, https://doi.org/10.1016/j.actao.2015.12.001.

  4. Balzarini, M.G., González, L., Tablada, M., Casanoves, F., Di Rienzo, J.A., Robledo, C.W., 2008. Infostat. Manual del Usuario, Editorial Brujas, Córdoba, Argentina., pp. 330–336.

  5. Banks, S.C., Finlayson, G.R., Lawson, S.J., Lindenmayer, D.B., Paetkau, D., Ward, S.J., Taylor, A.C., 2005. The effects of habitat fragmentation due to forestry plantation establishment on the demography and genetic variation of a marsupial carnivore, Antechinus agilis. Biol. Conserv. 122, 581–597, https://doi.org/10.1016/j.biocon.2004.09.013.

  6. Bilenca, D.N., Kravetz, F.O., 1998. Seasonal variations in microhabitat use and feeding habits of the pampas mouse Akodon azarae in agroecosystem of central Argentina. Acta Theriol. 43, 195–203, https://doi.org/10.4098/AT.arch.98-15.

  7. Bilenca, D.N., González-Fischer, C.M., Teta, P., Zamero, M., 2007. Agricultural intensification and small mammal assemblages in agroecosystems of the Rolling Pampas, central Argentina. Agricult. Ecosyst. Environ. 121, 371–375, https://doi.org/10.1016/j.agee.2006.11.014.

  8. Bilenca, D.N., Kravetz, P.O., Zuleta, G.A., 1992. Food habits of Akodon azarae and Calomys laucha (Cricetidae, Rodentia) in agroecosystems of central Argentina. Mammalia 56, 371–384, https://doi.org/10.1515/mamm.1992.56.3371.

  9. Bonatto, F., Coda, J., Gomez, D., Priotto, J., Steinmann, A., 2013. Inter-male aggression with regard to polygynous mating system in Pampean grassland mouse, Akodon azarae (Cricetidae: Sigmodontinae). J. Ethol. 31, 223–231, https://doi.org/10.1007/s10164-013-0370-4.

  10. Bonatto, F., Gomez, D., Steinmann, A., Priotto, J., 2012. Mating strategies of Pampean mouse males. Anim. Biol. 62, 381–396, https://doi.org/10.1163/157075612X634102.

  11. Bonatto, F., Priotto, J., Coda, J., Steinmann, A.R., 2017. Female intrasexual territoriality and its potential adaptive significance: the pampean grassland mouse as an ecological model species. Ethology 123, 230–241, https://doi.org/10.1111/eth.12592.

  12. Bonaventura, S.M., Kravetz, F., 1989. Relación roedorvegetación: Importanciade la disponibilidad de cobertura verde para Akodon azarae durante el invierno. Physis (Buenos Aires), Secc. C 47, 1–5.

  13. Bonnet, E., Van de Peer, Y., 2002. zt: a software tool for simple and partial mantel tests. J. Stat. Softw. 7, 1–12, https://doi.org/10.18637/jss.v007.i10.

  14. Busch, M., Kravetz, F.O., 1992. Competitive interactions among rodents (Akodon azarae, Calomys laucha, C musculinus and Oligoryzomys flavescens) in a two-habitat systems. I. Spacial and numerical relationships. Mammali 56, 45–56.

  15. Busch, M., Alvarez, M.R., Cittadino, E.A., Kravetz, F.O., 1997. Habitat selection and interspecific competition in rodents in Pampean agroecosystems. Mammalia 61, 167–184, https://doi.org/10.1515/mamm.1997.61.2.167.

  16. Busch, M., Bilenca, D.N., Cittadino, E.A., Cueto, G.R., 2005. Effect of removing a dominant competitor, Akodon azarae (Rodentia, Sigmodontinae) on community and population parameters of small rodent species in Central Argentina. Austral Ecol. 30, 168–178, https://doi.org/10.1111/j.1442-9993.2004.01434.

  17. Busch, M., Mino, M.H., Dadon, J.R., Hodara, K., 2001. Habitat selection by Akodon azarae and Calomys laucha (Rodentia, Muridae) in pampean agroecosystems. Mammalia 65, 29–48, https://doi.org/10.1515/mamm.2001.65.1.29.

  18. Cabrera, A., 1953. Esquema fitogeográfico de la República Argentina. Rev. Mus. La Plata. Bot. 8, 87–168.

  19. Cavia, R., Gómez Villafañe, I.E., Cittadino, E.A., Bilenca, D.N., Mino, M.H., Busch, M., 2005. Effects of cereal harvest on abundance and spatial distribution of the rodent Akodon azarae in central Argentina. Agric. Ecosyst. Environ. 107, 95–99, https://doi.org/10.1016/j.agee.2004.09.011.

  20. Centeno-Cuadros, A., Román, J., Delibes, M., Godoy, J.A., 2011. Prisoners in their habitat? Generalist dispersal by habitat specialists: a case study in Southern water vole (Arvicola sapidus). PLoS One 6, e24613, https://doi.org/10.1371/journal.pone.0024613.

  21. Chiappero, M.B., Sommaro, L.V., Priotto, J.W., Wiernes, M.P., Steinmann, A.R., Gardenal, C.N., 2016. Spatio-temporal genetic structure of the rodent Calomys venustus in linear, fragmented habitats. J. Mammal. 97, 424–435, https://doi.org/10.1093/jmammal/gyv186.

  22. Cittadino, E.A., De Carli, P., Busch, M., Kravetz, F.O., 1994. Effects of food supplementation on rodents in winter. J. Mammal. 75, 446–453, https://doi.org/10.2307/1382566.

  23. Clark, B.K., Clark, B.S., Johnson, L.A., Haynie, M.T., 2001. Influence of roads on movements of small mammals. Southwest. Nat. 46, 338, https://doi.org/10.2307/3672430.

  24. Coda, J., Gomez, D., Steinmann, A.R., Priotto, J., 2015. Small mammals in farmlands of Argentina: responses to organic and conventional farming. Agric. Ecosyst. Environ. 211, 17–23, https://doi.org/10.1016/j.agee.2015.05.007.

  25. Coulon, A., Cosson, J.F., Angibault, J.M., Cargnelutti, B., Galan, M., Morellet, N., Petit, E., Aulagnier, S., Hewison, A.J.M., 2004. Landscape connectivity influences gene flow in a roe deer population inhabiting a fragmented landscape: an individual-based approach. Mol. Ecol. 13 (9), 2841–2850, https://doi.org/10.1111/j.1365-294X.2004.02253.x.

  26. Cushman, S.A., Landguth, E.L., 2010. Spurious correlations and inference in landscape genetics. Mol. Ecol. 19(17), 3592–3602, https://doi.org/10.1111/j.1365-294X.2010.04656.x.

  27. Cushman, S.A., McKelvey, K.S., Hayden, J., Schwartz, M.K., 2006. Gene flow in complex landscapes: testing multiple hypotheses with causal modeling. Am. Nat. 168 (4), 486–499, https://doi.org/10.1086/506976.

  28. Dalby, P., 1975. Biology of pampa rodents. Balcarce area, Argentina. Publ. Mus. Mich. State Univ. Biol. Ser. 5, 149–272.

  29. de Villafañe, G., 1981. Reproduccióny crecimiento de Akodon azarae azarae (Fischer, 1829). Historia Natural (Argentina) 1, 193–204.

  30. Didham, R.K., 2010. The ecological consequences of habitat fragmentation. In: Encyclopedia of Life Sciences. John Wiley & Sons, Ltd, Chichester.

  31. Doerr, E.D., Doerr, V.A., Davies, M.J., McGinness, H.M., 2014. Does structural connectivity facilitate movement of native species in Australia’s fragmented landscapes? A systematic review protocol. Environ. Evid. 3, 1–8, https://doi.org/10.1186/2047-2382-3-9.

  32. Estes-Zumpf, W.A., Rachlow, J.L., Waits, L.P., Warheit, K.I., 2010. Dispersal, gene flow, and population genetic structure in the pygmy rabbit (Brachylagus idahoensis). J. Mammal. 91, 208–219, https://doi.org/10.1644/09-mamm-a-032r.1.

  33. Frankham, R., Briscoe, D.A., Ballou, J.D., 2002. Introduction to Conservation Genetics. Cambridge university press.

  34. Frantz, A.C., Hamann, J.L., Klein, F., 2008. Fine-scale genetic structure of red deer (Cervus elaphus) in a French temperate forest. Eur. J. Wildl. Res. 54, 44–52, https://doi.org/10.1007/s10344-007-0107-1.

  35. Ghersa, C.M., de la Fuente, E., Suarez, S., Leon, R.J.C., 2002. Woody species invasion in the Rolling Pampa. Agric. Ecosyst. Environ. 88, 271–278.

  36. Gomez, D., Sommaro, L., Steinmann, A., Chiappero, M., Priotto, J., 2011. Movement distances of two species of sympatric rodents in linear habitats of Central Argentine agroecosystems. Mamm. Biol. 76, 58–63, https://doi.org/10.1016/j.mambio.2010.02.001.

  37. Gomez, M.D., Coda, J., Simone, I., Martínez, J., Bonatto, F., Steinmann, A.R., Priotto, J., 2015. Agricultural land-use intensity and its effects on small mammals in the central region of Argentina. Mammal Res. 60, 415–423, https://doi.org/10.1007/s13364-015-0245-x.

  38. González-Ittig, R.E., Polop, F.J., Andreo, V.C, Chiappero, M.B., Levis, S., Calderón, G., Provensal, M.C, Polop, J.J., Gardenal, C.N., 2015. Temporal fine-scale genetic variation in the zoonosis-carrying long-tailed pygmy rice rat in Patagonia, Argentina. J. Zool. 296, 216–224, https://doi.org/10.1111/jzo.12238.

  39. Goudet, J., 2001. FSTAT, A Program to Estimate and Test Gene Diversities and Fixation Indices, Version 2.9.3. https://doi.org/www2.unil.ch/popgen/softwares/fstat.htm.

  40. Kierepka, E.M., Anderson, S.J., Swihart, R.K., Rhodes, O.E., 2016. Evaluating the influence of life-history characteristics on genetic structure: a comparison of small mammals inhabiting complex agricultural landscapes. Ecol. Evol. 6, 6376–6396, https://doi.org/10.1002/ece3.2269.

  41. Lancaster, M.L., Taylor, A.C., Cooper, S.J.B., Carthew, S.M., 2011. Limited ecological connectivity of an arboreal marsupial across a forest/plantation landscape despite apparent resilience to fragmentation. Mol. Ecol. 20, 2258–2271, https://doi.org/10.1111/j.1365-294X.2011.05072.x.

  42. Maniatis, T., Fritsch, E.F., Sambrook, J., 1982. Molecular Cloning: a Laboratory Manual, vol. 545. Cold spring harbor laboratory, Cold Spring Harbor, NY.

  43. Manuel-Navarrete, D., Gallopín, G., Blanco, M., Díaz-Zorita, M., Ferraro, D., Herzer, H., Laterra, P., Morello, J., Murmis, R., Pengue, W., Pineiro, M., Podestá, G., Satorre, H., Torrent, M., Torres, F., Viglizzo, E., Caputo, G., Celis, A., 2005. Análisis sistémico de la agriculturización en la pampa húmeda argentina y sus consecuencias en regiones extrapampeanas: Sostenibilidad, brechas de cnocimiento e integración de políticas,C EPAL- SERIE Medioambiente y Desarrollo, 118., pp. 1–65.

  44. McRae, B.H., Dickson, B.G., Keitt, T.H., Shah, V.B., 2008. Using circuit theory to model connectivity in ecology, evolution, and conservation. Mol. Ecol. 89, 2712–2724.

  45. Medan, D., Torretta, J.P., Hodara, K., de la Fuente, E.B., Montaldo, N.H., 2011. Effects of agriculture expansion and intensification on the vertebrate and invertebrate diversity in the Pampas of Argentina. Biodivers. Conserv. 20, 3077–3100, https://doi.org/10.1007/s10531-011-0118-9.

  46. Paruelo, J.M., Guerschman, J.P., Verón, S., 2005. Expansión agrícola y cambios en el uso del suelo. Cienc. Hoy 15, 14–23.

  47. Peakall, R.O.D., Smouse, P.E., 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6, 288–295.

  48. Peakall, R., Ruibal, M., Lindenmayer, D.B., 2003. Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus Fuscipes. Evolution 57, 1182–1195, https://doi.org/10.1111/j.0014-3820.2003.tb00327.x.

  49. Priotto, J.W., Steinmann, A.R., 1999. Factors affecting home range size and overlap in Akodon azarae (Muridae: Sigmodontinae) in natural pasture of Argentina. Acta Theriol. 44, 37–44.

  50. Priotto, J., Steinmann, A., Polop, J., 2002. Factors affecting home range size and overlap in Calomys venustus (Muridae: Sigmodontinae) in Argentine agroecosystems. Mamm. Biol. 67, 97–104, https://doi.org/10.1078/1616-5047-00014.

  51. Priotto, J.W., Polop, J., 1997. Space and time use in syntopic populations of Akodon azarae and Calomys venustus (Rodentia, Muridae). Z. Säugetierkunde 62, 30–36.

  52. Renner, S.C., Suarez-Rubio, M., Wiesner, K.R., Drögemüller, C., Gockel, S., Kalko, E.K., Frantz, A.C., 2016. Using multiple landscape genetic approaches totest the validity of genetic clusters in a species characterized by an isolation-by-distance pattern. Biol. J. Linn. Soc. 118 (2), 292–303, https://doi.org/10.1111/bij.12737.

  53. Rice, W.R., 1989. Analyzing tables of statistical tests. Evolution 43 (1), 223–225, https://doi.org/10.2307/2409177,22343.

  54. Schweizer, M., Excoffier, L., Heckel, G., 2007. Fine-scale genetic structure and dispersal in the common vole (Microtus arvalis). Mol. Ecol. 16, 2463–2473, https://doi.org/10.1111/j.1365-294X.2007.03284.x.

  55. Serafini, V.N., Priotto, J.W., Gómez, M.D., 2019. Effects of agroecosystem landscape complexity on small mammals: a multi-species approach at different spatial scales. Landscape Ecol. 34, 1117–1129, https://doi.org/10.1007/s10980-019-00825-8.

  56. Simone, I., Cagnacci, F., Provensal, C., Polop, J., 2010. Environmental determinants of the small mammal assemblage in an agroecosystem of central Argentina: the role of Calomys musculinus. Mamm. Biol. 75, 496–509, https://doi.org/10.1016/j.mambio.2009.12.002.

  57. Slatkin, M., 1985. Gene flow in natural populations. Ann. Rev. Ecol. Syst 16, 393–430, https://doi.org/10.1146/annurev.es.16.110185.002141.

  58. Sommaro, L.V., Ph D thesis 2012. Movimiento de Calomys musculinus en poblaciones naturales y experimentales. Facultas de Ciencias Exactas, Físico-Químico y Naturales. Universidad Nacional de Río Cuarto.

  59. Sommaro, L., Gomez, D., Bonatto, F., Steinmann, A., Chiappero, M., Priotto, J., 2010. Corn mice (Calomys musculinus) movement in linear habitats of agricultural ecosystems. J. Mammal. 91, 668–673, https://doi.org/10.1644/09-MAMM-A-232.1.

  60. Suárez, O.V., Ph D thesis 1996. Estrategias reproductivas y cuidado parental en Akodon azarae (Rodentia, Muridae). Universidad de Buenos Aires, Buenos Aires, Argentina.

  61. Taylor, A.C., Tyndale-Biscoe, H., Lindenmayer, D.B., 2007. Unexpected persistence on habitat islands: genetic signatures reveal dispersal of a eucalypt-dependent marsupial through a hostile pine matrix. Mol. Ecol. 16, 2655–2666, https://doi.org/10.1111/j.1365-294X.2007.03331.x.

  62. Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M., Shipley, P., 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4, 535–538, https://doi.org/10.1111/j.1471-8286.2004.00684.x.

  63. Vera, N.S., Chiappero, M.B., Priotto, J.W., Gardenal, C.N., 2011. Isolation of microsatellite loci in Akodon azarae (Muridae, Sigmodontinae) and cross-amplification in other Akodontini species. J. Genet. 92, 25–29, https://doi.org/10.1007/s12041-011-0044-3.

  64. Viglizzo, E., Lértora, F., Pordomingo, A., Bernardos, J., Roberto, Z., Del Valle, H., 2001. Ecological lessons and applications from one century of low external-input farming in the pampas of Argentina. Ecosyst. Environ. 83, 65–81, https://doi.org/10.1016/s0167-8809(00)00155-9.

  65. Volante, J., Mosciaro, J., Morales Poclava, M., Vale, L., Castrillo, S., Sawchik, J., Tiscornia, G., Fuente, M., Maldonado, I., Vega, A., Trujillo, R., Cortéz, L., Paruelo, J., 2015. Expansión agrícola en Argentina, Bolivia, Paraguay, Uruguay y Chile entre 2000-2010: Caracterización espacial mediante series temporales de índices de vegetación. RIA. Revista de investigaciones agropecuarias 41, 179–191.

  66. Weir, B.S., Cockerham, C.C., 1984. Estimating F-statistics for the analysis of population structure. Evolution (N.Y.) 38, 1358–1370, https://doi.org/10.2307/2408641.

  67. Zuleta, G.A., Ph D thesis 1989. Estrategia de historias de vida del ratón del pastizal pampeano, Akodon azarae. Facultad de ciencias exactas y naturales. Universidad Nacional de Buenos Aires.

  68. Zuleta, G.A., Bilenca, D.N., 1992. Seasonal shifts within juvenile recruit sex ratio of Pampas mice (Akodon azarae). J. Zool. 227 (3), 397–404.

  69. Zuleta, G., Kravetz, F.O., Busch, M.G.A. Zuleta, R.E., Bilenca, D.N., 1992. Seasonal shifts within juvenile recruit sex ratio of Pampas mice (Akodon azarae). J. Zool. 227 (3), 397–404.

  70. Zuleta, G., Kravetz, F.O., Busch, M., Percich, R.E., 1988. Dinámica poblacional del ratón del pastizal pampeano (Akodon azarae) en ecosistemas agrarios de Argentina. Revista Chilena de Historia Natural 61, 231–244.

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Vera, N.S., Chiappero, M.B., Priotto, J.W. et al. Genetic structure of populations of the Pampean grassland mouse, Akodon azarae, in an agroecosystem under intensive management. Mamm Biol 98, 52–60 (2019). https://doi.org/10.1016/j.mambio.2019.07.001

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Keywords

  • Akodon azarae
  • Spatial genetic autocorrelation
  • Microsatellite loci
  • Agroecosystem