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Journal Article

Asynchrony of Seasons: Genetic Differentiation Associated with Geographic Variation in Climatic Seasonality and Reproductive Phenology

Ignacio Quintero, Sebastián González-Caro, Paul-Camilo Zalamea and Carlos Daniel Cadena
The American Naturalist
Vol. 184, No. 3 (September 2014), pp. 352-363
DOI: 10.1086/677261
Stable URL: http://www.jstor.org/stable/10.1086/677261
Page Count: 12
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Abstract

AbstractMany organisms exhibit distinct breeding seasons tracking food availability. If conspecific populations inhabit areas that experience different temporal cycles in food availability spurred by variation in precipitation regimes, then they should display asynchronous breeding seasons. Thus, such populations might exhibit a temporal barrier to gene flow, which may potentially promote genetic differentiation. We test a central prediction of this hypothesis, namely, that individuals living in areas with more asynchronous precipitation regimes should be more genetically differentiated than individuals living in areas with more similar precipitation regimes. Using mitochondrial DNA sequences, climatic data, and geographical/ecological distances between individuals of 57 New World bird species mostly from the tropics, we examined the effect of asynchronous precipitation (a proxy for asynchronous resource availability) on genetic differentiation. We found evidence for a positive and significant cross-species effect of precipitation asynchrony on genetic distance after accounting for geographical/ecological distances, suggesting that current climatic conditions may play a role in population differentiation. Spatial asynchrony in climate may thus drive evolutionary divergence in the absence of overt geographic barriers to gene flow; this mechanism contrasts with those invoked by most models of biotic diversification emphasizing physical or ecological changes to the landscape as drivers of divergence.

Notes and References

This item contains 90 references.

Literature Cited
  • ['Adams, D. C. 2008. Phylogenetic meta-analysis. Evolution 62:567–572.']
  • ['Adriaensen, F., J. P. Chardon, G. De Blust, E. Swinnen, S. Villalba, H. Gulinck, and E. Matthysen. 2003. The application of “least-cost” modelling as a functional landscape model. Landscape and Urban Planning 64:233–247.']
  • ['Ahumada, J. A. 2001. Comparison of the reproductive biology of two Neotropical wrens in an unpredictable environment in northeastern Colombia. Auk 118:191–210.']
  • ['Alexander, R. D., and R. S. Bigelow. 1960. Allochronic speciation in field crickets, and a new species, Acheta veletis. Evolution 14:334–346.']
  • ['Barnes, J. B., T. A. Ehlers, N. Insel, N. McQuarrie, and C. J. Poulsen. 2012. Linking orography, climate, and exhumation across the central Andes. Geology 40:1135–1138.']
  • ['Bartholomé, E., and A. S. Belward. 2005. GLC2000: a new approach to global land cover mapping from Earth observation data. International Journal of Remote Sensing 26:1959–1977.']
  • ['Basist, A., G. D. Bell, and V. Meentemeyer. 1994. Statistical relationships between topography and precipitation patterns. Journal of Climate 7:1305–1315.']
  • ['Bloomfield, P. 2000. Fourier analysis of time series: an introduction. 2nd ed. Wiley, New York.']
  • ['Bralower, T. J., J. C. Zachos, E. Thomas, M. Parrow, C. K. Paull, D. C. Kelly, I. P. Silva, et al. 1995. Late Paleocene to Eocene paleoceanography of the equatorial Pacific Ocean: stable isotopes recorded at Ocean Drilling Program Site 865, Allison Guyot. Paleoceanography 10:841–865.']
  • ['Burger, C., and C. Both. 2011. Translocation as a novel approach to study effects of a new breeding habitat on reproductive output in wild birds. PLoS ONE 6:e18143.']
  • ['Burney, C., and R. Brumfield. 2009. Ecology predicts levels of genetic differentiation in Neotropical birds. American Naturalist 174:358–368.']
  • ['Bush, M. B. 2005. Of orogeny, precipitation, precession and parrots. Journal of Biogeography 32:1301–1302.']
  • ['Changnon, D., T. B. McKee, and N. J. Doesken. 1991. Hydroclimatic variability in the rocky Mountains. Journal of the American Water Resources Association 27:733–743.']
  • ['Charmantier, A., and P. Gienapp. 2014. Climate change and timing of avian breeding and migration: evolutionary versus plastic changes. Evolutionary Applications 7:15–28.']
  • ['Chiang, J. C. H., and C. M. Bitz. 2005. Influence of high latitude ice cover on the marine Intertropical Convergence Zone. Climate Dynamics 25:477–496.']
  • ['Coyne, J. A., and H. A. Orr. 2004. Speciation. Sinauer, Sunderland, MA.']
  • ['Crawley, M. J. 2007. The R book. 1st ed. Wiley, Chichester.']
  • ['Danner, J. E., R. M. Danner, F. Bonier, P. R. Martin, T. W. Small, and I. T. Moore. 2011. Female, but not male, tropical sparrows respond more strongly to the local song dialect: implications for population divergence. American Naturalist 178:53–63.']
  • ['Devaux, C., and R. Lande. 2008. Incipient allochronic speciation due to non-selective assortative mating by flowering time, mutation and genetic drift. Proceedings of the Royal Society B: Biological Sciences 275:2723–2732.']
  • ['Dittami, J. P., and E. Gwinner. 1985. Annual cycles in the African stonechat Saxicola torquata axillaris and their relationship to environmental factors. Journal of Zoology 207:357–370.']
  • ['Drummond A. J., B. Ashton, S. Buxton, M. Cheung, A. Cooper, C. Duran, M. Field, et al. 2010. Geneious, version 4.8. http://www.geneious.com.']
  • ['Dunn, P. O., D. W. Winkler, L. A. Whittingham, S. J. Hannon, and R. J. Robertson. 2011. A test of the mismatch hypothesis: how is timing of reproduction related to food abundance in an aerial insectivore? Ecology 92:450–461.']
  • ['Durant, J. M., D. Hjermann, G. Ottersen, and N. C. Stenseth. 2007. Climate and the match or mismatch between predator requirements and resource availability. Climate Research 33:271–283.']
  • ['Fagan, W. F., C. Cosner, E. A. Larsen, and J. M. Calabrese. 2010. Reproductive asynchrony in spatial population models: how mating behavior can modulate allee effects arising from isolation in both space and time. American Naturalist 175:362–373.']
  • ['Friesen, V. L., A. L. Smith, E. Gómez-Díaz, M. Bolton, R. W. Furness, J. González-Solés, and L. R. Monteiro. 2007. Sympatric speciation by allochrony in a seabird. Proceedings of the National Academy of Sciences of the USA 104:18589–18594.']
  • ['Gesch, D. B., K. L. Verdin, and S. K. Greenlee. 1999. New land surface digital elevation model covers the Earth. Eos, Transactions American Geophysical Union 80:69–70.']
  • ['Gill, F. B. 2007. Ornithology. 3rd ed. Freeman, New York.']
  • ['Goslee, S. C., and D. L. Urban. 2007. The ecodist package for dissimilarity-based analysis of ecological data. Journal of Statistical Software 22:1–19.']
  • ['Guillot, G., and F. Rousset. 2013. Dismantling the Mantel tests. Methods in Ecology and Evolution 4:336–344.']
  • ['Gutiérrez-Pinto, N., A. M. Cuervo, J. Miranda, J. L. Pérez-Emán, R. T. Brumfield, and C. D. Cadena. 2012. Non-monophyly and deep genetic differentiation across low-elevation barriers in a Neotropical montane bird (Basileuterus tristriatus; Aves: Parulidae). Molecular Phylogenetics and Evolution 64:156–165.']
  • ['Gwinner, E. 2003. Circannual rhythms in birds. Current Opinion in Neurobiology 13:770–778.']
  • ['Gwinner, E., and J. Dittami. 1990. Endogenous reproductive rhythms in a tropical bird. Science 249:906–908.']
  • ['Hahn, T. P., and S. A. MacDougall-Shackleton. 2008. Adaptive specialization, conditional plasticity and phylogenetic history in the reproductive cue response systems of birds. Philosophical Transactions of the Royal Society B: Biological Sciences 363:267–286.']
  • ['Hansen, T. F. 1997. Stabilizing selection and the comparative analysis of adaptation. Evolution 51:1341–1351.']
  • ['Hau, M., N. Perfito, and I. T. Moore. 2008. Timing of breeding in tropical birds: mechanisms and evolutionary implications. Ornitologia Neotropical 19:39–59.']
  • ['Helm, B. 2009. Geographically distinct reproductive schedules in a changing world: costly implications in captive stonechats. Integrative and Comparative Biology 49:563–579.']
  • ['Hendry, A. P., and T. Day. 2005. Population structure attributable to reproductive time: isolation by time and adaptation by time. Molecular Ecology 14:901–916.']
  • ['Hijmans, R. J. 2012. Cross-validation of species distribution models: removing spatial sorting bias and calibration with a null model. Ecology 93:679–688.']
  • ['———. 2013. raster: geographic data analysis and modeling. R package, version 2.1-16. http://CRAN.R-project.org/package=raster.']
  • ['Hijmans, R. J., S. E. Cameron, J. L. Parra, P. G. Jones, and A. Jarvis. 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25:1965–1978.']
  • ['Hijmans, R. J., S. Phillips, J. Leathwick, and J. Elith. 2013. dismo: species distribution modeling. R package, version 0.8-11. http://CRAN.R-project.org/package=dismo.']
  • ['Jacobs, J. D., and J. C. Wingfield. 2000. Endocrine control of life-cycle stages: a constraint on response to the environment? Condor 102:35–51.']
  • ['Jahn, A. E., D. J. Levey, A. M. Mamani, M. Saldias, A. Alcoba, M. J. Ledezma, B. Flores, et al. 2010. Diferencias entre temporadas en la lluvia, disponibilidad de comida y el comportamiento de forrajeo de Tyrannus melancholicus en el sur de la Cuenca Amazónica. Journal of Field Ornithology 81:340–348.']
  • ['Jetz, W., G. H. Thomas, J. B. Joy, K. Hartmann, and A. O. Mooers. 2012. The global diversity of birds in space and time. Nature 491:444–448.']
  • ['Kisel, Y., and T. G. Barraclough. 2010. Speciation has a spatial scale that depends on levels of gene flow. American Naturalist 175:316–334.']
  • ['Krishnamurti, T. N., L. Stefanova, and V. Misra. 2013. The intertropical convergence zone. Pages 35–46 in Tropical meteorology: an introduction. Springer, New York.']
  • ['Legates, D. R., and C. J. Willmott. 1990. Mean seasonal and spatial variability in gauge-corrected, global precipitation. International Journal of Climatology 10:111–127.']
  • ['Lofts, B. 1964. Evidence of an autonomous reproductive rhythm in an equatorial bird (Quelea quelea). Nature 201:523–524.']
  • ['Lofts, B., and R. K. Murton. 1968. Photoperiodic and physiological adaptations regulating avian breeding cycles and their ecological significance. Journal of Zoology 155:327–394.']
  • ['Malhi, Y., and J. Wright. 2004. Spatial patterns and recent trends in the climate of tropical rainforest regions. Philosophical Transactions of the Royal Society B: Biological Sciences 359:311–329.']
  • ['Martin, P. R., F. Bonier, I. T. Moore, and J. J. Tewksbury. 2009. Latitudinal variation in the asynchrony of seasons: implications for higher rates of population differentiation and speciation in the tropics. Ideas in Ecology and Evolution 2:9–17.']
  • ['Martin, R., L. Sebele, A. Koeslag, O. Curtis, and F. Abadi. 2014. Phenological shifts assist colonisation of a novel environment in a range-expanding raptor. Oikos. doi:10.1111/oik.01058.']
  • ['Martin, T. E. 1987. Food as a limit on breeding birds: a life-history perspective. Annual Review of Ecology and Systematics 18:453–487.']
  • ['Mayr, E. 1942. Systematics and the origin of species, from the viewpoint of a zoologist. Columbia University Press, New York.']
  • ['McRae, B. H., and P. Beier. 2007. Circuit theory predicts gene flow in plant and animal populations. Proceedings of the National Academy of Sciences of the USA 104:19885–19890.']
  • ['Moore, I. T., F. Bonier, and J. C. Wingfield. 2005. Reproductive asynchrony and population divergence between two tropical bird populations. Behavioral Ecology 16:755–762.']
  • ['Moore, M. C., H. Schwabl, and D. S. Farner. 1983. Biochronometry of testicular regression in white-crowned sparrows (Zonotrichia leucophrys gambelii). Journal of Comparative Physiology 153:489–494.']
  • ['Nelson, R. J. 2002. Seasonal patterns of stress, immune function, and disease. Cambridge University Press, Cambridge.']
  • ['Nussey, D. H., E. Postma, P. Gienapp, and M. E. Visser. 2005. Selection on heritable phenotypic plasticity in a wild bird population. Science 310:304–306.']
  • ['Oden, N. L., and R. R. Sokal. 1986. Directional autocorrelation: an extension of spatial correlograms to two dimensions. Systematic Biology 35:608–617.']
  • ['Orme, D., R. Freckleton, G. Thomas, T. Petzoldt, S. Fritz, N. Isaac, and W. Pearse. 2013. caper: comparative analyses of phylogenetics and evolution in R. R package, version 0.5. http://CRAN.R-project.org/package=caper.']
  • ['Paradis, E., J. Claude, and K. Strimmer. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290.']
  • ['Peterson, L. C., G. H. Haug, K. A. Hughen, and U. Röhl. 2000. Rapid changes in the hydrologic cycle of the tropical Atlantic during the last glacial. Science 290:1947–1951.']
  • ['Pianka, E. R. 1969. Habitat specificity, speciation, and species density in Australian desert lizards. Ecology 50:498–502.']
  • ['Posada, D. 2008. JModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25:1253–1256.']
  • ['Poulin, B., G. Lefebvre, and R. McNeil. 1992. Tropical avian phenology in relation to abundance and exploitation of food resources. Ecology 73:2295–2309.']
  • ['Quintero, I., S. González-Caro, P. Zalamea, and C. D. Cadena. 2014. Data from: Asynchrony of seasons: genetic differentiation associated with geographic variation in climatic seasonality and reproductive phenology. American Naturalist, Dryad Digital Repository, http://dx.doi.org/10.5061/dryad.40d6h.']
  • ['R Core Team. 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.']
  • ['Revell, L. J. 2010. Phylogenetic signal and linear regression on species data. Methods in Ecology and Evolution 1:319–329.']
  • ['Ricklefs, R. E., and G. Bloom. 1977. Components of avian breeding productivity. Auk 94:86–96.']
  • ['Ritchie, M. G. 2001. Chronic speciation in periodical cicadas. Trends in Ecology and Evolution 16:59–61.']
  • ['Saerens, M., Y. Achbany, F. Fouss, and L. Yen. 2009. Randomized shortest-path problems: two related models. Neural Computation 21:2363–2404.']
  • ['Scheuerlein, A., and E. Gwinner. 2002. Is food availability a circannual zeitgeber in tropical birds? a field experiment on stonechats in tropical Africa. Journal of Biological Rhythms 17:171–180.']
  • ['Shine, R., and G. P. Brown. 2008. Adapting to the unpredictable: reproductive biology of vertebrates in the Australian wet-dry tropics. Philosophical Transactions of the Royal Society B: Biological Sciences 363:363–373.']
  • ['Simon, C., J. Tang, S. Dalwadi, G. Staley, J. Deniega, and T. R. Unnasch. 2000. Genetic evidence for assortative mating between 13-year cicadas and sympatric “17-year cicadas with 13-year life cycles” provides support for allochronic speciation. Evolution 54:1326–1336.']
  • ['Stotz, D. F., J. W. Fitzpatrick, T. A. Parker III, and D. K. Moskovits. 1996. Neotropical birds: ecology and conservation. University of Chicago Press, Chicago.']
  • ['Swofford, D. 2003. PAUP*, version 4. Sinauer, Sunderland, MA.']
  • ['Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28:2731–2739.']
  • ['Valderrama, E., J. L. Pérez-Emán, R. T. Brumfield, A. M. Cuervo, and C. D. Cadena. 2014. The influence of the complex topography and dynamic history of the montane Neotropics on the evolutionary differentiation of a cloud forest bird (Premnoplex brunnescens, Furnariidae). Journal of Biogeography 41:1533–1546.']
  • ['van Etten, J. 2012. gdistance: distances and routes on geographical grids. R package, version 1.1-4. http://CRAN.R-project.org/package=gdistance.']
  • ['van Schaik, C. P., J. W. Terborgh, and S. J. Wright. 1993. The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annual Review of Ecology and Systematics 24:353–377.']
  • ['Versteegh, M. A., B. Helm, E. Gwinner, and B. I. Tieleman. 2012. Annual cycles of metabolic rate are genetically determined but can be shifted by phenotypic flexibility. Journal of Experimental Biology 215:3459–3466.']
  • ['Weir, J. T. 2009. Implications of genetic differentiation in Neotropical montane forest birds. Annals of the Missouri Botanical Garden 96:410–433.']
  • ['Wikelski, M., M. Hau, and J. C. Wingfield. 2000. Seasonality of reproduction in a Neotropical rain forest bird. Ecology 81:2458–2472.']
  • ['Wingfield, J. C., T. P. Hahn, R. Levin, and P. Honey. 1992. Environmental predictability and control of gonadal cycles in birds. Journal of Experimental Zoology 261:214–231.']
  • ['Wingfield, J. C., R. E. Hegner, J. Dufty, and G. F. Ball. 1990. The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. American Naturalist 136:829–846.']
  • ['Wright, S. J., and O. Calderón. 2006. Seasonal, El Niño and longer term changes in flower and seed production in a moist tropical forest. Ecology Letters 9:35–44.']
  • ['Yamamoto, S., and T. Sota. 2009. Incipient allochronic speciation by climatic disruption of the reproductive period. Proceedings of the Royal Society B: Biological Sciences 276:2711–2719.']
  • ['———. 2012. Parallel allochronic divergence in a winter moth due to disruption of reproductive period by winter harshness. Molecular Ecology 21:174–183.']
  • ['Zalamea, P.-C., F. Munoz, P. R. Stevenson, C. E. T. Paine, C. Sarmiento, D. Sabatier, and P. Heuret. 2011. Continental-scale patterns of Cecropia reproductive phenology: evidence from herbarium specimens. Proceedings of the Royal Society B: Biological Sciences 278:2437–2445.']
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