Correlated morphological and genetic patterns in Embothrium coccineum (Proteaceae) across climate and geography: can Embothrium survive patagonian climate change?
Cintia P. Souto A C and Peter E. Smouse B
+ Author Affiliations
- Author Affiliations
A Laboratorio Ecotono, Universidad Nacional del Comahue, Quintral 1250, Bariloche 8400, Argentina.
B Department of Ecology, Evolution and Natural Resources, Rutgers University, New Brunswick, NJ 08901, USA.
C Corresponding author. Email: cintia.souto@crub.uncoma.edu.ar
Australian Journal of Botany 61(7) 516-527 https://doi.org/10.1071/BT13214
Submitted: 29 August 2013 Accepted: 9 October 2013 Published: 11 February 2014
Abstract
Adaptive radiation and reproductive isolation can determine the biogeographic structure of any species. We examine patterns of biotic variation in Embothrium coccineum, a Proteaceae tree that spans 20° of latitude and is both morphologically and genetically highly variable. We aim to (1) explore the correspondence between these biotic patterns and current geographic and climatic gradients, and (2) determine whether and how those patterns are likely to respond to changing climate. We conducted separate principal component analyses on biotic and abiotic sets of variables for 34 populations of Embothrium coccineum, accounting for a large fraction of the total variation in each. We then used canonical correlation analyses to optimise the match of those gradients onto each other. Smaller, rounder leaves and particular alleles typify the colder and drier parts of the range, whereas larger, lanceolate leaves and other alleles typify warmer and moister areas. Finally, we mapped biotic profiles onto a predicted climatic landscape, on the basis of doubling of CO2 projections. The climatic regime is predicted to shift geographically, but this lineage has successfully responded to repeated and dramatic climatic shifts since the Oligocene, and it should also be able to move and adapt quickly enough to meet the present challenge. More generally, our analytic approach can be extended to analysis of biotic and abiotic patterns in other species facing climatic challenges. Where there is enough biogeographic variation to provide adaptively relevant substrate, and where propagule dispersal is sufficiently extensive to keep up with the pace of spatial climatic shift, such taxa should be able to cope with shifting climate.
Additional keywords: climatic gradients, genetic variation, geographic metrics, multivariate analysis, phenotypic patterns.
References
Blanchet FG, Legendre P, Borcard D (2008) Forward selection of explanatory variables. Ecology 89, 2623–2632.| Forward selection of explanatory variables.Crossref | GoogleScholarGoogle Scholar | 18831183PubMed |
Britten HB, Brussard PF, Murphy DD, Ehrlich PR (1995) A test for isolation-by-distance in central Rocky Mountain and Great Basin populations of Edith’s checkerspot butterfly (Euphydryas editha). The Journal of Heredity 86, 204–210.
Broughton RE, Harrison RG (2003) Nuclear gene genealogies reveal historical, demographic and selective factors associated with speciation in field crickets. Genetics 163, 1389–1401.
Canale CI, Henry PI (2010) Adaptive phenotypic plasticity and resilience of vertebrates to increasing climatic unpredictability. Climate Research 43, 135–147.
| Adaptive phenotypic plasticity and resilience of vertebrates to increasing climatic unpredictability.Crossref | GoogleScholarGoogle Scholar |
Clausen J, Keck DD, Hiesey WM (1940) ‘Experimental studies on the nature of species. I. The effect of varied environments on western North American plants.’ Publication no. 520. (Carnegie Institution: Washington, DC)
CONAMA (2007) Estudio de la variabilidad climática en Chile para el siglo XXI. Available at http://www.dgf.uchile.cl/PRECIS/articles- 39442_pdf_Informe_figuras.pdf [Verified 1 November 2013]
Daniels LD, Veblen TT (2000) ENSO effects on temperature and precipitation of the Patagonian-Andean region: implications for biogeography. Physical Geography 21, 223–243.
Davis MB, Shaw RG (2001) Range shifts and adaptive responses to quaternary climate change. Science 292, 673–679.
| Range shifts and adaptive responses to quaternary climate change.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjt1elsrY%3D&md5=911d0c9a8bcc68003e4c161461046898CAS | 11326089PubMed |
DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends in Ecology & Evolution 13, 77–81.
| Costs and limits of phenotypic plasticity.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFygsQ%3D%3D&md5=c2921018201307b5a219a53d37680954CAS |
Dilcher DL (1973) A paleoclimatic interpretation of the Eocene floras of southeastern North America. In ‘Vegetation and vegetational history of northern Latin America’. (Ed. A. Graham) pp. 39–59. (Elsevier Scientific Publishing Company: Amsterdam)
Dolph GE, Dilcher DL (1980) Variation in leaf size with respect to climate in the tropics of the western hemisphere. Bulletin of the Torrey Botanical Club 107, 154–162.
| Variation in leaf size with respect to climate in the tropics of the western hemisphere.Crossref | GoogleScholarGoogle Scholar |
Endler JA (1986) ‘Natural selection in the wild.’ (Princeton University Press: Princeton, NJ)
Epperson BK (1993) Recent advances in correlation studies of spatial patterns of genetic variation. Evolutionary Biology 27, 95–155.
| Recent advances in correlation studies of spatial patterns of genetic variation.Crossref | GoogleScholarGoogle Scholar |
Escobar B, Donoso C, Souto C, Alberdi M, Zúñiga A (2006) Embothrium coccineum. In ‘Las especies arbóreas de los bosques templados de Chile y Argentina: autoecología’. (Ed. C. Donoso) pp. 233–245. (Marisa Cuneo Ediciones: Valdivia, Chile)
ESRI (2008) ArcGIS Version 9.3. Environmental Systems Research Institute, Redlands, CA.
Gaggiotti OE, Foll M (2010) Quantifying population structure with the F-model. Molecular Ecology Resources 10, 821–830.
| Quantifying population structure with the F-model.Crossref | GoogleScholarGoogle Scholar | 21565093PubMed |
Galloway LF (2005) Maternal effects provide phenotypic adaptation to local environmental conditions. New Phytologist 166, 93–100.
| Maternal effects provide phenotypic adaptation to local environmental conditions.Crossref | GoogleScholarGoogle Scholar | 15760354PubMed |
Gienapp P, Teplitsky C, Alho JS, Mills JA, Merilä J (2008) Climate change and evolution: disentangling environmental and genetic responses. Molecular Ecology 17, 167–178.
| Climate change and evolution: disentangling environmental and genetic responses.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1c%2Fgsl2muw%3D%3D&md5=c8c217d9b66ecaa28dd0634de38633caCAS | 18173499PubMed |
Givnish TJ (1979) On the adaptive significance of leaf form. In ‘Topics in plant population biology’. (Eds OT Solbrig, S Jain, GB Johnsonand, PH Raven) pp. 375–407. (Columbia University Press: New York)
Govindasamy B, Caldeira K, Duffy PB (2003) Geoengineering Earth’s radiation balance to mitigate climate change from a quadrupling of CO2. Global and Planetary Change 37, 157–168.
| Geoengineering Earth’s radiation balance to mitigate climate change from a quadrupling of CO2.Crossref | GoogleScholarGoogle Scholar |
Hamrick JL, Nason JD (1996) Consequences of dispersal in plants. In ‘Population dynamics in ecological space and time’. (Eds OE Rhodes, RK Chesser, MH Smith) pp. 203–236. (University of Chicago: Chicago, IL)
Hardy J, Vanderhoeven S, Meerts P, Vekemans X (2000) Spatial autocorrelation of allozyme and quantitative markers within a natural population of Centaurea jacea (Asteraceae). Journal of Evolutionary Biology 13, 656–667.
| Spatial autocorrelation of allozyme and quantitative markers within a natural population of Centaurea jacea (Asteraceae).Crossref | GoogleScholarGoogle Scholar |
Hijmans RJ, Guarino L, Cruz M, Rojas E (2001) Computer tools for spatial analysis of plant genetic resources data: 1. DIVA-GIS. Plant Genetic Resources Newsletter 127, 15–19.
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25, 1965–1978.
| Very high resolution interpolated climate surfaces for global land areas.Crossref | GoogleScholarGoogle Scholar |
Hill RS (2004) Origins of the southeastern Australian vegetation. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 359, 1537–1549.
Holt RD (1990) The microevolutionary consequences of climate change. Trends in Ecology & Evolution 5, 311–315.
| The microevolutionary consequences of climate change.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7hsValtA%3D%3D&md5=eab8d48b6633a0844b3a09ed4f1e0b07CAS |
Houghton JT, Ding Y, Griggs DJ, Noguer M, van der Linden PJ, Dai X, Maskell K, Johnson CA (2001) ‘Climate change 2001: the scientific basis.’ Contribution of Working Group 1 to the third assessment report of the intergovernmental panel on climate change. (Cambridge University Press: Cambridge, UK)
Legendre P, Legendre L. (1998) ’Numerical ecology.’ Elsevier.
Linhart YB, Grant MRC (1996) Evolutionary significance of local genetic differentiation. Annual Review of Ecology and Systematics 27, 237–277.
| Evolutionary significance of local genetic differentiation.Crossref | GoogleScholarGoogle Scholar |
Maddox GD, Antonovics J (1983) Experimental ecological genetics in Plantago: a structural equation approach to fitness components in P. aristata and P. patagonica. Ecology 64, 1092–1099.
| Experimental ecological genetics in Plantago: a structural equation approach to fitness components in P. aristata and P. patagonica.Crossref | GoogleScholarGoogle Scholar |
Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends in Ecology & Evolution 15, 290–295.
Manel S, Joost S, Epperson BK (2010) Perspectives on the use of landscape genetics to detect genetic adaptive variation in the field. Molecular Ecology 19, 3760–3772.
| Perspectives on the use of landscape genetics to detect genetic adaptive variation in the field.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1aqsrzL&md5=c024ba0fe5ee01200ceb143623740ef2CAS | 20723056PubMed |
Markgraf V, McGlone M, Hope G (1995) Neogene paleoenvironmental and paleoclimatic change in southern temperate ecosystems – a southern perspective. Trends in Ecology & Evolution 10, 143–147.
| Neogene paleoenvironmental and paleoclimatic change in southern temperate ecosystems – a southern perspective.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFajug%3D%3D&md5=1ca4c53c95a5579cd87f9b04c8f0048aCAS |
Mathiasen P, Premoli AC (2010) Out in the cold: genetic variation of Nothofagus pumilio (Nothofagaceae) provides evidence for latitudinally distinct evolutionary histories in austral South America. Molecular Ecology 19, 371–385.
| Out in the cold: genetic variation of Nothofagus pumilio (Nothofagaceae) provides evidence for latitudinally distinct evolutionary histories in austral South America.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktlOntLY%3D&md5=7bc549e6178b0b50e1944264fa149bf0CAS | 20002584PubMed |
Mitton JB (1995) Genetics and the physiological ecology of conifers. In ‘Ecophysiology of coniferous forests’. (Ed. TM Hinckley) pp. 1–36. (Academic Press: New York)
Montecinos A, Aceituno P (2003) Seasonality of the ENSO related rainfall variability in central Chile and associated circulation anomalies. Journal of Climate 16, 281–296.
| Seasonality of the ENSO related rainfall variability in central Chile and associated circulation anomalies.Crossref | GoogleScholarGoogle Scholar |
Morton NE (1973) Isolation by distance. In ‘Genetic structure of populations’. (Ed. NE Morton) pp. 76–79. (University Press of Hawaii: Honolulu, HI)
Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42.
| A globally coherent fingerprint of climate change impacts across natural systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXoslM%3D&md5=721ae9c1a87c8a413a652951b47a8021CAS | 12511946PubMed |
Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308, 1912–1915.
| Climate change and distribution shifts in marine fishes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlsVWmtbg%3D&md5=aeeb734f3c597625fa5ffad8db6f7038CAS | 15890845PubMed |
Pigliucci M, Whitton J, Schlichting CD (1995) Reaction norms of Arabidopsis. I. Plasticity of characters and correlations across water, nutrient and light gradients. Journal of Evolutionary Biology 8, 421–438.
| Reaction norms of Arabidopsis. I. Plasticity of characters and correlations across water, nutrient and light gradients.Crossref | GoogleScholarGoogle Scholar |
Reich PB, Walters MB, Tjoelker MG, Vanderklein D, Buschena C (1998) Photosynthesis and respiration rates depend on leaf and root morphology and nitrogen concentration in nine boreal tree species differing in relative growth rate. Functional Ecology 12, 395–405.
| Photosynthesis and respiration rates depend on leaf and root morphology and nitrogen concentration in nine boreal tree species differing in relative growth rate.Crossref | GoogleScholarGoogle Scholar |
Sauquet H, Weston PH, Anderson CA, Barker NP, Cantrill DJ, Mast AR, Savolainen V (2009) Contrasted patterns of hyperdiversification in Mediterranean hotspots. Proceedings of the National Academy of Sciences, USA 106, 221–225.
| Contrasted patterns of hyperdiversification in Mediterranean hotspots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltF2ksw%3D%3D&md5=256c19593b46a537732560d0fb664a3aCAS |
Schluter D, Rambaut A (1996) Ecological speciation in postglacial fishes. Proceedings of the Royal Society of London. Series B, Biological Sciences 351, 807–814. [and discussion]
Smouse PE, Long JC (1992) Matrix correlation analysis in anthropology and genetics. Yearbook of Physical Anthropology 35, 187–213.
| Matrix correlation analysis in anthropology and genetics.Crossref | GoogleScholarGoogle Scholar |
Smouse PE, Long JC, Sokal RR (1986) Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Systematic Zoology 35, 627–632.
| Multiple regression and correlation extensions of the Mantel test of matrix correspondence.Crossref | GoogleScholarGoogle Scholar |
Sokal RR, Wartenberg DE (1983) A test of spatial autocorrelation analysis using an isolation-by-distance model. Genetics 105, 219–237.
Sork VL, Stowe KA, Hochwender C (1993) Evidence for local adaptation in closely adjacent subpopulations of northern red oak (Quercus rubra L.) expressed as resistance for leaf herbivores. American Naturalist 142, 928–936.
| Evidence for local adaptation in closely adjacent subpopulations of northern red oak (Quercus rubra L.) expressed as resistance for leaf herbivores.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1Mzjt1GitQ%3D%3D&md5=167d6124c3b003785a2488646ad9d715CAS | 19425941PubMed |
Sork VL, Davis FW, Westfall R, Flint A, Ikegami M, Wang H, Grivet D (2010) Gene movement and genetic association with regional climate gradients in California valley oak (Quercus lobata Née) in the face of climate change. Molecular Ecology 19, 3806–3823.
| Gene movement and genetic association with regional climate gradients in California valley oak (Quercus lobata Née) in the face of climate change.Crossref | GoogleScholarGoogle Scholar | 20723054PubMed |
Soto A, Robledo-Arnuncio JJ, González-Martínez SC, Smouse PE, Alía R (2010) Climatic niche and neutral genetic diversity of the six Iberian pine species: a retrospective and prospective view. Molecular Ecology 19, 1396–1409.
| Climatic niche and neutral genetic diversity of the six Iberian pine species: a retrospective and prospective view.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3czisVagtA%3D%3D&md5=f11a20bd216bb6e77d9fd6e94fb74dadCAS | 20196810PubMed |
Souto CP, Premoli AC (2007) Genetic variation in the widespread Embothrium coccineum (Proteaceae) endemic to Patagonia: effects of phylogeny and historical events. Australian Journal of Botany 55, 809–817.
| Genetic variation in the widespread Embothrium coccineum (Proteaceae) endemic to Patagonia: effects of phylogeny and historical events.Crossref | GoogleScholarGoogle Scholar |
Souto CP, Premoli AC, Reich PB (2009) Complex bioclimatic and soil gradients shape leaf trait variation in Embothrium coccineum (Proteaceae) among austral forests in Patagonia. Revista Chilena de Historia Natural 82, 209–222.
| Complex bioclimatic and soil gradients shape leaf trait variation in Embothrium coccineum (Proteaceae) among austral forests in Patagonia.Crossref | GoogleScholarGoogle Scholar |
Telles MPC, Diniz-Filho JAF (2005) Multiple Mantel tests and isolation-by-distance, taking into account long-term historical divergence. Genetics and Molecular Research 4, 742–748.
Watterson R (1978) The homozygosity test of neutrality. Genetics 88, 405–417.
Webb LJ (1968) Environment relationships of the structural types of Australian rainforest vegetation. Ecology 49, 296–311.
| Environment relationships of the structural types of Australian rainforest vegetation.Crossref | GoogleScholarGoogle Scholar |
Westoby M (1998) A leaf-height-seed (LHS) plant ecology strategy scheme. Plant and Soil 199, 213–227.
| A leaf-height-seed (LHS) plant ecology strategy scheme.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjslOht7o%3D&md5=94eeecae2a3e41951cf516572a56f852CAS |
Wilf P, Wing SL, Greenwood DR, Greenwood CL (1998) Using fossil leaves as paleoprecipitation indicators: an Eocene example. Geology 26, 203–206.
| Using fossil leaves as paleoprecipitation indicators: an Eocene example.Crossref | GoogleScholarGoogle Scholar |
Wilkinson C, Edds D (2001) Spatial pattern and environmental correlates of a midwestern stream fish assemblage: including spatial autocorrelation as a factor in community analyses. American Midland Naturalist 146, 271–289.
| Spatial pattern and environmental correlates of a midwestern stream fish assemblage: including spatial autocorrelation as a factor in community analyses.Crossref | GoogleScholarGoogle Scholar |
Wright S (1943) Isolation by distance. Genetics 28, 114–138.
