The Paradox of Forest Fragmentation Genetics
La Paradoja de la Genética de la Fragmentación de Bosques
ANDREA T. KRAMER
Department of Biological Sciences (M/C 066), University of Illinois at Chicago, 845 W. Taylor Street, Chicago, IL 60607, U.S.A.
Chicago Botanic Garden, Division of Plant Science and Conservation, 1000 Lake Cook Road, Glencoe, IL 60022, U.S.A.
Search for more papers by this authorJENNIFER L. ISON
Department of Biological Sciences (M/C 066), University of Illinois at Chicago, 845 W. Taylor Street, Chicago, IL 60607, U.S.A.
Chicago Botanic Garden, Division of Plant Science and Conservation, 1000 Lake Cook Road, Glencoe, IL 60022, U.S.A.
Search for more papers by this authorMARY V. ASHLEY
Department of Biological Sciences (M/C 066), University of Illinois at Chicago, 845 W. Taylor Street, Chicago, IL 60607, U.S.A.
Search for more papers by this authorCorresponding Author
HENRY F. HOWE
Department of Biological Sciences (M/C 066), University of Illinois at Chicago, 845 W. Taylor Street, Chicago, IL 60607, U.S.A.
Department of Zoology, Field Museum of Natural History, 1400 S. Lake Shore Drive, Chicago, IL 60605, U.S.A.
§Address correspondence to H. F. Howe, email [email protected]Search for more papers by this authorANDREA T. KRAMER
Department of Biological Sciences (M/C 066), University of Illinois at Chicago, 845 W. Taylor Street, Chicago, IL 60607, U.S.A.
Chicago Botanic Garden, Division of Plant Science and Conservation, 1000 Lake Cook Road, Glencoe, IL 60022, U.S.A.
Search for more papers by this authorJENNIFER L. ISON
Department of Biological Sciences (M/C 066), University of Illinois at Chicago, 845 W. Taylor Street, Chicago, IL 60607, U.S.A.
Chicago Botanic Garden, Division of Plant Science and Conservation, 1000 Lake Cook Road, Glencoe, IL 60022, U.S.A.
Search for more papers by this authorMARY V. ASHLEY
Department of Biological Sciences (M/C 066), University of Illinois at Chicago, 845 W. Taylor Street, Chicago, IL 60607, U.S.A.
Search for more papers by this authorCorresponding Author
HENRY F. HOWE
Department of Biological Sciences (M/C 066), University of Illinois at Chicago, 845 W. Taylor Street, Chicago, IL 60607, U.S.A.
Department of Zoology, Field Museum of Natural History, 1400 S. Lake Shore Drive, Chicago, IL 60605, U.S.A.
§Address correspondence to H. F. Howe, email [email protected]Search for more papers by this authorAbstract
enAbstract: Theory predicts widespread loss of genetic diversity from drift and inbreeding in trees subjected to habitat fragmentation, yet empirical support of this theory is scarce. We argue that population genetics theory may be misapplied in light of ecological realities that, when recognized, require scrutiny of underlying evolutionary assumptions. One ecological reality is that fragment boundaries often do not represent boundaries for mating populations of trees that benefit from long-distance pollination, sometimes abetted by long-distance seed dispersal. Where fragments do not delineate populations, genetic theory of small populations does not apply. Even in spatially isolated populations, where genetic theory may eventually apply, evolutionary arguments assume that samples from fragmented populations represent trees that have had sufficient time to experience drift, inbreeding, and ultimately inbreeding depression, an unwarranted assumption where stands in fragments are living relicts of largely unrelated predisturbance populations. Genetic degradation may not be as important as ecological degradation for many decades following habitat fragmentation.
Abstract
esResumen: La teoría predice una gran pérdida de diversidad genética por deriva y endogamia de árboles sujetos a la fragmentación de hábitat; sin embargo, el soporte empírico de esta teoría es escaso. Argumentamos que la teoría de la genética de poblaciones puede ser mal aplicada a la luz de realidades ecológicas que, al ser reconocidas, requieren del escrutinio de los supuestos evolutivos subyacentes. Una realidad ecológica es que los límites de los fragmentos a menudo no representan los límites para las poblaciones de árboles que se benefician con la polinización a larga distancia, a veces favorecida por la dispersión de semillas a larga distancia. Donde los fragmentos no delinean poblaciones, la teoría genética de las poblaciones pequeñas no aplica. Aun en poblaciones espacialmente aisladas, donde la teoría genética eventualmente puede aplicar, los argumentos evolutivos asumen que las muestras de poblaciones fragmentadas representan árboles que han tenido suficiente tiempo para experimentar deriva, endogamia y, finalmente, depresión por endogamia, una suposición que carece de base y donde los individuos de los fragmentos son relictos vivientes de poblaciones no emparentadas antes de la perturbación. La degradación genética puede no ser tan importante como la degradación ecológica durante muchas décadas después de la fragmentación del hábitat.
Literature Cited
- Aizen, M. A., and P. Feinsinger. 1994. Forest fragmentation, pollination, and plant reproduction in a chaco dry forest, Argentina. Ecology 75: 330–351.
- Aldrich, P. R., and J. L. Hamrick. 1998. Reproductive dominance of pasture trees in a fragmented tropical forest mosaic. Science 281: 103–105.
- Apsit, V. J., J. L. Hamrick, and J. D. Nason. 2001. Breeding population size of a fragmented population of a Costa Rican dry forest tree species. Journal of Heredity 92: 415–420.
- Asquith, N. 2001. Misdirections in conservation biology. Conservation Biology 15: 345–352.
- Bacles, C. F. E., A. J. Lowe, and R. A. Ennos. 2004. Genetic effects of chronic habitat fragmentation on tree species: the case of Sorbus aucuparia in a deforested Scottish landscape. Molecular Ecology 13: 573–584.
- Bacles, C. F. E., J. Burczyk, A. J. Lowe, and R. A. Ennos. 2005. Historical and contemporary mating patterns in remnant populations of the forest tree Fraxinus excelsior L. Evolution 59: 979–990.
- Bacles, C. F. E., A. J. Lowe, and R. A. Ennos. 2006. Effective seed dispersal across a fragmented landscape. Science 311: 628.
- Ballal, S. R., S. A. Fore, and S. I. Guttman. 1994. Apparent gene flow and genetic-structure of Acer saccharum subpopulations in forest fragments. Canadian Journal of Botany 72: 1311–1315.
- Bond, W. 1994. Do mutualisms matter? Assessing the impact of pollinator and disperser disruption on plant extinction. Philosophical Transactions: Biological Sciences 344: 83–90.
- Bormann, F. H., T. G. Siccama, G. E. Likens, and R. H. Whittaker. 1970. The Hubbard Brook ecosystem study: composition and dynamics of the tree stratum. Ecological Monographs 40: 373–388.
- Boshier, D. H., J. E. Gordon, and A. J. Barrance. 2004. Prospects for Circa situm tree conservation in Mesoamerican dry forest agroecosystems. University of California Press, Berkeley, California .
- Caughley, G. 1994. Directions in conservation biology. Journal of Animal Ecology 63: 215–244.
- Chase, M. R., C. Moller, R. Kesseli, and K. S. Bawa. 1996. Distant gene flow in tropical trees. Nature 383: 398–399.
- Clark, J., M. Silman, R. Kern, E. Macklin, and J. HilleRisLambers. 1999. Seed dispersal near and far: Patterns across temperate and tropical forests. Ecology 80: 1475–1494.
- Collevatti, R. G., D. Grattapaglia, and J. D. Hay. 2001. Population genetic structure of the endangered tropical tree species Caryocar brasiliense, based on variability at microsatellite loci. Molecular Ecology 10: 349–356.
- Cordeiro, N., and H. Howe. 2001. Low recruitment of trees dispersed by animals in African forest fragments. Conservation Biology 15: 1733–1741.
- Cordeiro, N. J., and H. F. Howe. 2003. Forest fragmentation severs mutualism between seed dispersers and an endemic African tree. Proceedings of the National Academy of Sciences of the United States of America 100: 14052–14056.
- Craft, K. J., and M. V. Ashley. 2007. Landscape genetic structure of bur oak (Quercus macrocarpa) savannas in Illinois. Forest Ecology and Management 239: 13–20.
- Cunningham, S. A. 2000. Effects of habitat fragmentation on the reproductive ecology of four plant species in Mallee woodland. Conservation Biology 14: 758–768.
- Daily G. C., P. R. Ehrlich, and G. A. Sánchez-Azofeifa. 2001. Countryside biogeography: utilization of human dominated habitats by the avifauna of southern Costa Rica. Ecological Applications 11: 1–13.
- Dick, C. W. 2001. Genetic rescue of remnant tropical trees by an alien pollinator. Proceedings of the Royal Society of London Series B-Biological Sciences 268: 2391–2396.
- Dick, C. W., G. Etchelecu, and F. Austerlitz. 2003. Pollen dispersal of tropical trees (Dinizia excelsa: Fabaceae) by native insects and African honeybees in pristine and fragmented Amazonian rainforest. Molecular Ecology 12: 753–764.
- Didham, R. K., J. Ghazoul, N. E. Stork, and A. J. Davis. 1996. Insects in fragmented forests: a functional approach. Trends in Ecology & Evolution 11: 255–260.
- Dow, B. D., and M. V. Ashley. 1996. Microsatellite analysis of seed dispersal and parentage of saplings in bur oak, Quercus macrocarpa. Molecular Ecology 5: 615–627.
- Dow, B. D., and M. V. Ashley. 1998. High levels of gene flow in bur oak revealed by paternity analysis using microsatellites. The Journal of Heredity 89: 62–70.
- Estrada, A., and R. Coates-Estrada. 2002. Bats in continuous forest, forest fragments and in an agricultural mosaic habitat-island at Los Tuxtlas, Mexico. Biological Conservation 103: 237–245.
- Fore, S. A., R. J. Hickey, J. L. Vankat, S. I. Guttman, and R. L. Schaefer. 1992. Genetic structure after forest fragmentation: a landscape ecology perspective on Acer saccharum. Canadian Journal of Botany 70: 1659–1668.
- Gaiotto, F. A., D. Grattapaglia, and R. Vencovsky. 2003. Genetic structure, mating system, and long-distance gene flow in heart of palm (Euterpe edulis Mart.). Journal of Heredity 94: 399–406.
- Ghazoul, J. 2005. Pollen and seed dispersal among dispersed plants. Biological Reviews 80: 413–443.
- Ghazoul, J., and M. McLeish. 2001. Reproductive ecology of tropical forest trees in logged and fragmented habitats in Thailand and Costa Rica. Plant Ecology 153: 335–345.
- Gonzalez-Martinez, S. C., J. Burczyk, R. Nathan, N. Nanos, L. Gil, and R. Alia. 2006. Effective gene dispersal and female reproductive success in Mediterranean maritime pine (Pinus pinaster Aiton). Molecular Ecology 15: 4577–4588.
- Goto, S., K. Shimatani, H. Yoshimaru, and Y. Takahashi. 2006. Fat-tailed gene flow in the dioecious canopy tree species Fraxinus mandshurica var. japonica revealed by microsatellites. Molecular Ecology 15: 2985–2996.
- Hall, P., M. R. Chase, and K. S. Bawa. 1994. Low genetic-variation but high population differentiation in a common tropical forest tree species. Conservation Biology 8: 471–482.
- Hall, P., S. Walker, and K. Bawa. 1996. Effect of forest fragmentation on genetic diversity and mating system in a tropical tree, Pithecellobium elegans. Conservation Biology 10: 757–768.
- Hardesty, B. D., S. P. Hubbell, and E. Bermingham. 2006. Genetic evidence of frequent long-distance recruitment in a vertebrate-dispersed tree. Ecology Letters 9: 516–525.
- Heilman, G. E., Jr., J. R. Strittholt, N. C. Slosser, and D. A. DellaSala. 2002. Forest fragmentation of the conterminous United States: assessing forest intactness through road density and spatial characteristics. BioScience 52: 411–422.
- Holbrook, K. M., T. B. Smith and B. D. Hardesty. 2002. Implications of long-distance movements of frugivorous rain forest hornbills. Ecography 25: 745–749.
- Horvitz, C., and D. Schemske. 1990. Spatiotemporal variation in insect mutualists of a Neotropical herb. Ecology 71: 1085–1097.
- Hubbell, S. P. 2001. The unified neutral theory of biodiversity and biogeography. Princeton University Press, Princeton , New Jersey.
- Hubbell, S. P., and R. B. Foster. 1983. Diversity of canopy trees in a Neotropical forest and implications for conservation. Pages 25–41 in S. Sutton, T. C. Whitmore, and A. Chadwick, editors. Tropical rain forest: ecology and management. Blackwell Publishing, Oxford , United Kingdom .
- Hufford K. M., and J. L. Hamrick. 2003. Viability selection at three early life stages of the tropical tree, Platypodium elegans (Fabaceae, Papilionoideae). Evolution 57: 518–526.
- Husband, B. C., and D. W. Schemske. 1996. Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50: 54–70.
- Ingle, N. R. 2003. Seed dispersal by wind, birds and bats between Philippine montane rainforest and successional vegetation. Oecologia 134: 251–261.
- Jones, F. A., J. Chen, G. J. Weng, and S. P. Hubbell. 2005. A genetic evaluation of seed dispersal in the Neotropical tree Jacaranda copaia (Bignoniaceae). The American Naturalist 166: 543–555.
- Jordano, P., and J. A. Godoy. 2002. Frugivore-generated seed shadows: a landscape view of demographic and genetic effects. Pages 305–321 in D. J. Levey, W. Silva, and M. Galetti, editors. Frugivores and seed dispersal: ecological, evolutionary, and conservation perspectives. CAB International, Wallingford , United Kingdom .
- Jump, A. S., and J. Penuelas. 2006. Genetic effects of chronic habitat fragmentation in a wind-pollinated tree. Proceedings of the National Academy of Sciences of the United States of America 103: 8096–8100.
- Kenta, T., Y. Isagi, M. Nakagawa, M. Yamashita, and T. Nakashizuka. 2004. Variation in pollen dispersal between years with different pollination conditions in a tropical emergent tree. Molecular Ecology 13: 3575–3684.
- Knapp, E. E, M. A. Goedde, and K. J. Rice. 2001. Pollen-limited reproduction in blue oak: implications for wind pollination in fragmented populations. Oecologia 128: 48–55.
- Latouche-Halle, C., A. Ramboer, E. Bandou, H. Caron, and A. Kremer. 2004. Long-distance pollen flow and tolerance to selfing in a Neotropical tree species. Molecular Ecology 13: 1055–1064.
- Lowe, A. J., D. Boshier, D. Ward, C. F. E. Bacles, and C. Navarro. 2005. Genetic resource impacts of habitat loss and degradation; reconciling empirical evidence and predicted theory for Neotropical trees. Heredity 95: 256–273.
- Magurran, A. 2004. Measuring biological diversity. Blackwell Publishing, Oxford , United Kingdom .
- Maina, G., and H. F. Howe. 2000. Inherent rarity in community restoration. Conservation Biology 14: 1335–1340.
- Martínez-Garza, C., and González-Montagut, R. 1999. Seed rain from forest fragments into tropical pastures in Los Tuxtlas, Mexico. Plant Ecology 145: 255–265.
- Matsuki, Y., Y. Isagi, and Y. Suyama. 2007. The determination of multiple microsatellite genotypes and DNA sequences from a single pollen grain. Molecular Ecology Notes 7: 194–198.
- McConkey, K. R., and D. R. Drake. 2002. Extinct pigeons and declining bat populations: are large seeds still being dispersed in the tropical Pacific? Pages 381–395 in D. J. Levey, W. Silva, and M. Galetti, editors. Frugivores and seed dispersal: ecological, evolutionary, and conservation perspectives. CAB International, Wallingford , United Kingdom .
- Nakanishi, A., N. Tomaru, H. Yoshimaru, T. Kawahara, T. Manabe, and S. Yamamoto. 2004. Patterns of pollen flow and genetic differentiation among pollen pools in Quercus salicina in a warm temperate old-growth evergreen broad-leaved forest. Silvae Genetica 53: 258–264.
- Nason, J. D., and J. L. Hamrick. 1997. Reproductive and genetic consequences of forest fragmentation: two case studies of Neotropical canopy trees. Journal of Heredity 88: 264–276.
- Nason, J. D., E. A. Herre, and J. L. Hamrick. 1998. The breeding structure of a tropical keystone plant resource. Nature 391: 685–687.
- O'Connell, L. M., A. Mosseler, and O. P. Rajora. 2006a. Impacts of forest fragmentation on the reproductive success of white spruce (Picea glauca). Canadian Journal of Botany 84: 956–965.
- O'Connell, L. M., A. Mosseler, and O. P. Rajora. 2006b. Impacts of forest fragmentation on the mating system and genetic diversity of white spruce (Picea glauca) at the landscape level. Heredity 97: 418–426.
- Peres, C. A. 2001. Synergistic effects of subsistence hunting and habitat fragmentation on Amazonian forest vertebrates. Conservation Biology 15: 1490–1505.
- Pitman, N. C. A., J. Terborgh, M. R. Silman, P. Nunez V., D. A. Neill, C. E. Ceron, W. A. Palacios, and M. Aulestia. 2001. Dominance and distribution of tree species in upper Amazonian terra firme forests. Ecology 82: 2101–2117.
- Preston, F. W. 1948. The commonness, and rarity, of species. Ecology 29: 254–283.
- Prober, S. M., and A. H. D. Brown. 1994. Conservation of the grassy white box woodlands: population genetics and fragmentation of Eucalyptus albens. Conservation Biology 8: 1003–1013.
- Quesada, M., K. E. Stoner, J. A. Lobo, Y. Herrerias-Diego, C. Palacios-Guevara, M. A. Munguia-Rosas, K. A. O.-Salazar, and V. Rosas-Guerrero. 2004. Effects of forest fragmentation on pollinator activity and consequences for plant reproductive success and mating patterns in bat-pollinated Bombacaceous trees. Biotropica 36: 131–138.
- Robledo-Arnuncio, J. J., and L. Gil. 2005. Patterns of pollen dispersal in a small population of Pinus sylvestris L. revealed by total exclusion paternity analysis. Heredity 94: 13–22.
- Sato, T., Y. Isagi, H. Sakio, K. Osumi, and S. Goto. 2006. Effect of gene flow on spatial genetic structure in the riparian canopy tree Cercidiphyllum japonicum revealed by microsatellite analysis. Heredity 96: 79–84.
- Schuster, W. S. F., and J. B. Mitton. 2000.Paternity and gene dispersal in limber pine (Pinus flexilis James). Heredity 84: 348–361.
- Streiff, R., A. Ducousso, C. Lexer, H. Steinkellner, J. Gloessl, and A. Kremer. 1999. Pollen dispersal inferred from paternity analysis in a mixed oak stand of Quercus robur L. and Q. petraea (Matt.) Liebl. Molecular Ecology 8: 831.
- Vakkari, P., A. Blom, M. Rusanen, J. Raisio, and H. Toivonen. 2006. Genetic variability of fragmented stands of pedunculate oak (Quercus robur) in Finland. Genetica 127: 231–241.
- Westcott, D. A., J. Bentrupperbäumer, M. G. Bradford, and A. McKeown. 2005. Incorporating patterns of disperser behaviour into models of seed dispersal and its effects on estimated dispersal curves. Oecologia 146: 57–67.
- White, G. M., D. H. Boshier, and W. Powell. 2002. Increased pollen flow counteracts fragmentation in a tropical dry forest: an example from Swietenia humilis Zuccarini. Proceedings of the National Academy of Sciences of the United States of America 99: 2038–2042.
- Young, A., T. Boyle, and T. Brown. 1996. The population genetic consequences of habitat fragmentation for plants. Trends in Ecology & Evolution 11: 413–418.
- Young, A. G., and H. G. Merriam. 1994. Effects of forest fragmentation on the spatial genetic-structure of Acer saccharum marsh populations. Heredity 72: 201–208.