Spatial Mating Networks In Insect-pollinated Plants

Gene flow in plant populations is largely determined by landscape heterogeneity. Both the shape of the pollination kernel and the spatial distribution of trees affect the distribution of pollen grains and the genotypes they harbour, but little is known about the relative contribution of each of these two factors. Using genetic markers we build a spatial network of pollination events between any two trees in a population of Prunus mahaleb, an insect-pollinated plant. Then, we apply tools from the science of complex networks to characterize the structure of such a mating network. Although the distribution of the number of pollen donors per tree is quite homogeneous, the identity of donors is distributed heterogeneously across the population. This results in a population structured in well-defined modules or compartments, formed by a group of mother trees and their shared pollen donors. Long-distance pollination events decrease the modular structure by favouring mating among all available mates. This increases gene flow across the entire population, reducing its genetic structure, and potentially decreasing the role of genetic drift. © 2008 Blackwell Publishing Ltd/CNRS.115490498Albert, R., Barabási, A.-L., Jeong, H., Error and attack tolerance in complex networks (2000) Nature, 406, pp. 378-382Austerlitz, F., Smouse, P.E., Two-generation analysis of pollen flow across a landscape. II. Relation between Phi(ft), pollen dispersal and interfemale distance (2001) Genetics, 157, pp. 851-857Austerlitz, F., Dick, C.W., Dutech, C., Klein, E.K., Oddou-Muratorio, S., Smouse, P.E., Using genetic markers to estimate the pollen dispersal curve (2004) Mol. Ecol., 13, pp. 937-954Barrett, S.C.H., Harder, L.D., Ecology and evolution of plant mating (1996) Trends Ecol. Evol., 11, pp. A73-A79Bascompte, J., Networks in ecology (2007) Basic Appl. Ecol., 8, pp. 485-490Campbell Grant, E.H., Lowe, W.H., Fagan, W.F., Living in the branches: Population dynamics and ecological processes in dendritic networks (2007) Ecol. Lett., 10, pp. 165-175Dyer, R.J., Nason, J., Population graphs: The graph theoretic shape of genetic structure (2004) Mol. Ecol., 13, pp. 1713-1727Epperson, B.K., (2003) Geographical Genetics., , Princeton University Press, PrincetonFortuna, M.A., Gómez-Rodríguez, C., Bascompte, J., Spatial network structure and amphibian persistence in stochastic environments (2006) Proc. R. Soc. Lond. B, 273, pp. 1429-1434García, C., Arroyo, J.M., Godoy, J.A., Jordano, P., Mating patterns, pollen dispersal, and the ecological maternal neighbourhood in a Prunus mahaleb population (2005) Mol. Ecol., 14, pp. 1821-1830García, C., Jordano, P., Godoy, J.A., Contemporary pollen and seed dispersal patterns and the spatial genetic structure in a Prunus mahaleb population (2007) Mol. Ecol., 16, pp. 1947-1955Gérard, P.R., Klein, E.K., Austerlitz, F., Fernández- Manjarrés, J.F., Frascaria-Lacoste, N., Assortative mating and differential male mating success in an ash hybrid zone population (2006) BMC Evol. Biol., 6, p. 96Godoy, J.A., Jordano, P., Seed dispersal by animals: Exact identification of source trees with endocarp DNA microsatellites (2001) Mol. Ecol., 10, pp. 2275-2283Guimerà, R., Amaral, L.A.N., Functional cartography of complex metabolic networks (2005) Nature, 433, pp. 895-900Hamrick, J.L., Murawski, D.A., Nason, J.D., The influence of seed dispersal mechanisms on the genetic structure of tropical tree populations (1993) Vegetatio, 107-108, pp. 281-297Jordano, P., Pollination biology of Prunus mahaleb deferred consequences of gender variation for fecundity and seed size (1993) Biol. J. Linnean Soc., 50, pp. 65-84Jordano, P., Godoy, J.A., Frugivore-generated seed shadows: A landscape view of the demographic and genetic effects (2002) Seed Dispersal and Frugivory: Ecology, Evolution, and Conservation, pp. 305-321. , In: eds. Levey, D.J., Silva, W.R. Galetti, M.). CABI Publishing, Wallingford, UK, ppKirkpatrick, S., Gelatt Jr., C.D., Vecchi, M.P., Optimization by simulated annealing (1983) Science, 220, pp. 671-680Klein, E.K., Lavinge, C., Gouyan, P.-H., Mixing of propagules from discrete sources at long distances: Comparing a dispersal tail to an exponential (2006) BMC Ecol., 6, p. 3Liepelt, S., Bialozyt, R., Ziegenhagen, B., Wind-dispersed pollen mediates postglacial gene flow among refugia (2002) Proc. Natl. Acad. Sci. USA, 99, pp. 14590-14594Liljeros, F., Edling, C.R., Amaral, L.A.N., Stanley, H.E., Aberg, Y., The web of human sexual contacts (2001) Nature, 411, pp. 907-908May, R.M., Network structure and the biology of populations (2006) Trends Ecol. Evol., 21, pp. 394-399Meagher, T.R., Vassiliadis, C., Spatial geometry determines gene flow in plant populations (2003) Genes in Environment: 15th Special Symposium of the British Ecological Society, pp. 76-90. , In: eds. Hails, R., Beringer, J. Godfray, H.C.). British Ecological Society, London, ppNewman, M.E.J., The structure of scientific collaboration networks (2001) Proc. Natl. Acad. Sci. USA, 98, pp. 404-409Newman, M.E.J., Modularity and community structure in networks (2006) Proc. Natl. Acad. Sci. USA, 113, pp. 8577-8582Newman, M.E.J., Girvan, M., Finding and evaluating community structure in networks (2004) Phys. Rev. e, 69, p. 026113Proulx, S.R., Promislow, D.E.L., Phillips, P.C., Network thinking in ecology and evolution (2005) Trends Ecol. Evol., 20, pp. 345-353Robledo-Arnuncio, J.J., Alia, R., Gil, L., Increased selfing and correlated paternity in a small population of a predominantly outcrossing conifer, Pinus sylvestris (2004) Mol. Ecol., 13, pp. 2567-2577Rosvall, M., Bergstrom, C.T., An information-theoretic framework for resolving community structure in complex networks (2007) Proc. Natl. Acad. Sci. USA, 104, pp. 7327-7331Savolainen, O., Pyhäjärvi, T., Knürr, T., Gene flow and local adaptation in trees (2007) Ann. Rev. Ecol. Syst., 38, pp. 595-619Schick, R.S., Lindley, S., Directed connectivity among fish populations in a riverine network (2007) J. Appl. Ecol., 44, pp. 1116-1126Sork, V.L., Nason, J., Campbell, D.R., Fernandez, J.F., Landscape approaches to historical and contemporary gene flow in plants (1999) Trends Ecol. Evol., 14, pp. 219-224Urban, D., Keitt, T., Landscape connectivity: A graph-theoretic perspective (2001) Ecology, 82, pp. 1205-121