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Population Genetics of Manihot Esculenta Ssp

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Population Genetics of Manihot Esculenta Ssp CORE Metadata, citation and similar papers at core.ac.uk Provided by Archive Ouverte en Sciences de l'Information et de la Communication This is a postprint version of a paper published in Molecular Ecology (2009) 18:2897-2907; doi: 10.1111/j.1365- 294X.2009.04231.x and available on the publisher’s website. POPULATION GENETICS OF MANIHOT ESCULENTA SSP. FLABELLIFOLIA GIVES INSIGHT INTO PAST DISTRIBUTION OF XERIC VEGETATION IN A POSTULATED FOREST REFUGIUM AREA IN NORTHERN AMAZONIA Anne Duputié 1, 2, Marc Delêtre 3, Jean-Jacques de Granville 4, Doyle McKey 1 The Guianas have often been proposed as a forest refugium; however, this view has received little testing. Studies of population genetics of forest taxa suggest that the central part of French Guiana remained forested, while the southern part (currently forested) may have harboured more open vegetation. Insights into the population structure of species restricted to non-forested habitats can help test this hypothesis. Using six microsatellite loci, we investigated the population genetics of French Guianan accessions of Manihot esculenta ssp. flabellifolia, a taxon restricted to coastal savannas and to rocky outcrops in the densely forested inland. Coastal populations were highly differentiated from one another, and our data suggest a recent colonization of these savannas by M. esculenta ssp. flabellifolia in a west-to-east process. Coastal populations were strongly differentiated from inselberg populations, consistent with an ancient separation of these two groups, with no or low subsequent gene flow. This supports the hypothesis that the central part of the region may have remained forested since the last glacial maximum, impeding the establishment of Manihot. Contrary to coastal populations, inselberg Manihot populations were strikingly homogeneous, at a broad spatial scale. This suggests they were connected until recently, either by a large continuous savanna area, or by smaller, temporary disturbed areas shifting in space. 1 CEFE UMR5175, 1919 Route de Mende, 34293 Montpellier Cedex 5, France 2 Corresponding author. Email: [email protected] 3 Botany Department, School of Natural Sciences, Trinity College Dublin, Dublin 2, Ireland 4 Unité 84 Biodival, Institut de Recherche pour le Développement, Herbier de Guyane, Route de Montabo, BP165, 97323 Cayenne Cedex, France This is a postprint version of a paper published in Molecular Ecology (2009) 18:2897-2907; doi: 10.1111/j.1365-294X.2009.04231.x and available on the publisher’s website. last glacial maximum. Introduction Phylogeogeographic studies may provide insights into past Climate variation due to Milankovitch oscillations has vegetation. To cast light on the history of the vegetation of the triggered repeated shifts in species distributions (Hewitt 2000). Guianas, we examined the population genetics of a plant During glacial periods, climate in the tropics was cooler and drier restricted to dry environments, at the scale of French Guiana. than now, whereas it was warmer and wetter during interglacials The species we considered, Manihot esculenta ssp. flabellifolia (Hewitt 2000). Several theories explaining patterns of species (Pohl) Ciferri, is the wild progenitor of cassava (Olsen & Schaal distribution in Amazonia have been proposed. On the one hand, 1999), with which it has been shown to occasionally hybridize in the long-debated refugia theory proposed by Haffer (1969) nature, at least in the coastal savannas of French Guiana postulates that forests have expanded during interglacials, and (Duputié et al. 2007). Manihot esculenta ssp. flabellifolia is receded during glacial times, becoming restricted to small islands distributed on an arc partly encircling the Amazon basin, from (refugia) in a matrix of savanna vegetation or dry forest eastern Bolivia and Peru eastward to northeastern Brazil, (Pennington et al. 2000). Allopatric speciation of forest species northward to the Guianas and then westward to Venezuela. In would have been favoured by such stable forest refugia, and the the southwestern part of its distribution range, the plant grows regions of high forest species endemism, such as the Guianas in transition zones between forest and cerrado and can persist as (Haffer 1969; de Granville 1982; de Granville et al. 1993; Bush a climbing shrub growing in openings in the forest (Allem 1994; 1994), would have been forest refugia. On the other hand, Olsen & Schaal 1999), but it also grows as a bushy shrub in open Bush’s (1994) disturbance-vicariance hypothesis proposes that areas in this region (A. Duputié, D. McKey, pers. obs.). In the high endemism in the Guianas is due not to long-term stability of northeastern part of its distribution range, the taxon is found in this region, but to numerous climate changes in this region. High open environments such as savannas and granitic outcrops. Its endemism would be due to high rates of speciation, favoured by distribution range in the Guianas is very patchy, as it is found in a selection pressures due to environmental change. According to narrow stretch along the coast, and forms small populations on this view, vegetation adapted to drier climates covered much of rocky outcrops (inselbergs) far away from the coast, a the Guianas during glacial times, with rainforest expanding distribution pattern it shares with numerous other species during interglacials. restricted to dry environments (de Granville 1982). In inner Data supporting one or the other hypothesis in the Guianas French Guiana, where forest openings and river banks could are scarce. We are aware of only one site in inner French Guiana offer suitable habitats, Manihot esculenta ssp. flabellifolia has where palynological studies have been conducted, in the central never been found. It is also absent from inselbergs located in part of French Guiana (Charles-Dominique et al. 1998; Ledru northeastern French Guiana (Figure 1). 2001). This site remained forested for the last 10,000 years In contrast to cassava, which farmers propagate clonally (Charles-Dominique et al. 1998), although primary forest was using stem cuttings, vegetative reproduction appears to play no temporarily replaced by secondary forest at least twice, around role in the biology of Manihot esculenta ssp. flabellifolia. 1,500 BP and around 1,000 BP (Ledru 2001). Results of charcoal Observations suggest that the taxon is pollinated mostly by analyses conducted on soil cores (Tardy 1998), together with meliponine bees. Seeds are dispersed first by ballistic autochory, those arising from population genetic studies of a rainforest tree through explosive dehiscence of the fruit, and then are species, Vouacapoua americana (Dutech et al. 2003, 2004), were secondarily dispersed by ants (notably Ectatomma brunneum consistent with this central region being a forest refugium since and Dorymyrmex pyramicus ssp. guyanensis in the Guianas [Elias the Last Glacial Maximum (LGM). However, no studies so far & McKey 2000]). Seeds germinate in response to disturbance have considered the remote southern part of French Guiana, and/or opening of the environment (Pujol et al. 2002). As which is characterized by a drier forest type than in the meliponine bees have a flight range of only 0.1 - 1 km (Roubik remainder of the country (Gond et al. 2005). Vegetation models 1989), and as seed dispersal does not exceed a few meters (Elias for the LGM suggest that the central part of French Guiana, as 2000), most dispersal events occur over a very short range. well as the western coastal region, were covered by rainforest Because the germination of Manihot esculenta ssp. flabellifolia is vegetation during the LGM, whereas southern and eastern conditioned to canopy opening, and as its closest relatives are regions harboured somewhat drier vegetation [either dry forest restricted to open environments (Duputié et al., unpubl. data), or savannas; Bush (1994); van der Hammen & Hooghiemstra one can hypothesize that this taxon has been restricted to open (2000); Pennington et al. (2006)]. However, climate simulations environments over the past few thousand years. by Mayle et al. (2004) infer the continuous presence of Genetic characteristics of Manihot populations from coastal evergreen broad-leaved forest in the whole region ever since the and inner French Guiana may help cast light on the history of This is a postprint version of a paper published in Molecular Ecology (2009) 18:2897-2907; doi: 10.1111/j.1365-294X.2009.04231.x and available on the publisher’s website. vegetation in this part of Amazonia. If the northern part of the and coastal populations of Manihot in this region. To that aim, it region (excluding the coastal savanna corridor) has remained is first necessary to assess whether, and to what extent, gene forested during the past few thousand years, as postulated by flow from domesticated cassava has affected the genome of its Haffer (1969), de Granville (1982) and Dutech et al. (2004), one wild relative in French Guiana. should expect this zone to have formed a barrier to the dispersal of Manihot esculenta ssp. flabellifolia. Populations from the Material & Methods coastal savannas should therefore be strongly differentiated from populations of inner savannas. If the southern part of the Sampling region also remained forested, as Haffer (1969) postulated, species restricted to dry environments should have been Leaf samples were picked from 373 individuals of Manihot historically restricted to small xeric islands (inselbergs). Under esculenta ssp. flabellifolia (sensu Allem 1994) from all over this scenario, populations of M. esculenta ssp. flabellifolia in the French Guiana, between 2002 and 2007. Ten populations were southern part of the region would have been founded through sampled along the coast and four on inselbergs (filled squares on occasional long-distance colonization of a few migrants. Hence, a Figure 1; sampling locations are presented in greater detail in strong isolation by distance should be expected for the inselberg Supplementary Table 1). One of these, SM, is the population populations of southern French Guiana. These populations where hybrids with cassava had been found by Duputié et al.
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