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Patterns of Pollen Dispersal in a Small Population of the Canarian Endemic Palm (Phoenix Canariensis)

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Patterns of Pollen Dispersal in a Small Population of the Canarian Endemic Palm (Phoenix Canariensis) Heredity (2014) 113, 215–223 & 2014 Macmillan Publishers Limited All rights reserved 0018-067X/14 www.nature.com/hdy ORIGINAL ARTICLE Patterns of pollen dispersal in a small population of the Canarian endemic palm (Phoenix canariensis) I Saro1, JJ Robledo-Arnuncio2, MA Gonza´lez-Pe´rez1 and PA Sosa1 The genetic diversity of small populations is greatly influenced by local dispersal patterns and genetic connectivity among populations, with pollen dispersal being the major component of gene flow in many plants species. Patterns of pollen dispersal, mating system parameters and spatial genetic structure were investigated in a small isolated population of the emblematic palm Phoenix canariensis in Gran Canaria island (Canary Islands). All adult palms present in the study population (n ¼ 182), as well as 616 seeds collected from 22 female palms, were mapped and genotyped at 8 microsatellite loci. Mating system analysis revealed an average of 5.8 effective pollen donors (Nep) per female. There was strong variation in correlated paternity rates across maternal progenies (ranging from null to 0.9) that could not be explained by the location and density of local males around focal females. Paternity analysis revealed a mean effective pollen dispersal distance of B71 m, with B70% of effective pollen originating from a distance of o75 m, and 90% from o200 m. A spatially explicit mating model indicated a leptokurtic pollen dispersal kernel, significant pollen immigration (12%) from external palm groves and a directional pollen dispersal pattern that seems consistent with local altitudinal air movement. No evidence of inbreeding or genetic diversity erosion was found, but spatial genetic structure was detected in the small palm population. Overall, the results suggest substantial pollen dispersal over the studied population, genetic connectivity among different palm groves and some resilience to neutral genetic erosion and subsequently to fragmentation. Heredity (2014) 113, 215–223; doi:10.1038/hdy.2014.16; published online 12 March 2014 INTRODUCTION the fraction of sibling pairs that share the same father) and the The evolutionary dynamics of plants depends on gene flow within probability of identity of two uniting gametes within a population and among populations, the patterns of which largely influence (that is, the inverse of the ‘neighbourhood size’, sensu Wright, 1943; spatial genetic structuring (Loveless and Hamrick, 1984; Smouse and see Crawford, 1984; Robledo-Arnuncio and Austerlitz, 2006; Pluess Sork, 2004). At the microevolutionary level, gene flow by pollen et al., 2009). Short-distance pollen dispersal can be efficiently assessed dispersal is a major determinant of mating patterns, within-popula- via paternity analysis of parent–offspring genotypic samples (Jones tion genetic diversity and among-population connectivity in spatially et al., 2010) that also allows investigating the effect of phenotypic structured plant species, counteracting the effect of isolation by traits and ecological variables on individual male reproductive success distance (Wright, 1943). Of particular concern is the loss of genetic (Nielsen et al., 2001; Oddou-Muratorio et al.,2003).Rarelong- diversity potentially resulting from mate limitation and gene flow distance pollen dispersal events, on the other hand, although much disruptions associated with population size reduction (Jump and harder to detect and quantify, are the vector of genetic connectivity Pen˜uelas, 2006). However, some mechanisms such as effective pollen among populations, especially across fragmented landscapes and seed dispersal and traits such as the longevity of trees could (Trakhtenbrot et al., 2005; Klein et al., 2006), that bears potentially increase their resilience to the negative effects of small population size important consequences for local adaptation in changing environ- (Hamrick, 2004; Jump and Pen˜uelas, 2006). Thus, assessing spatial ments (Kremer et al.,2012). patterns of pollen movement, as well as their interaction with mating Although accurately estimating the frequency and origin of long- systems, pollination syndromes and ecological and demographic distance effective pollen dispersal events remains an enormous factors has become an important topic in experimental ecological experimental challenge (Kremer et al., 2012), local paternity analysis and evolutionary studies, especially with the availability of highly can provide some hints on its frequency through the estimation of polymorphic microsatellite markers (Smouse et al.,2001;Burczyk pollen immigration rates into isolated populations and the examina- et al., 2002; Robledo-Arnuncio et al., 2006). Mating distance tion of the shape of the tail of (locally) estimated dispersal functions distributions typically exhibit an excess of nearby events (Levin and (Burczyk et al., 2002; Austerlitz et al., 2004; Oddou-Muratorio et al., Kerster, 1974), a short-distance component of effective pollen 2005; Klein et al., 2006). One of the most frequent approaches to dispersal that greatly determines correlated paternity rates (that is, estimate local mating patterns is maximum-likelihood categorical 1Grupo de Biogeografı´a, Conservacio´ n y Territorio, Universidad de Las Palmas de Gran Canaria (ULPGC), Las Palmas de Gran Canaria, Gran Canaria, Canary Islands, Spain and 2Department of Forest Ecology and Genetics, Forest Research Center (CIFOR), INIA, Madrid, Spain Correspondence: I Saro, Departamento de Biologı´a, Campus de Tafira, Universidad de Las Palmas de Gran Canaria, Las Palmas de Gran Canaria, Gran Canaria, Canary Island 35017, Spain. E-mail: [email protected] Received 29 June 2013; revised 20 December 2013; accepted 23 January 2014; published online 12 March 2014 Patterns of pollen dispersal in P. canariensis ISaroet al 216 paternity assignment (see, for example, Marshall et al., 1998) that palm population; (2) investigate phenotypic and ecological correlates enables individually explicit characterization of effective pollen of individual mating system parameters; and (3) assess patterns of dispersal at the cost of frequently large numbers of unassigned fine-scale spatial genetic structure of a small natural isolated Canarian offspring and substantial type II errors (Oddou-Muratorio et al., palm population. 2003). Fractional paternity analysis (see, for example, Nielsen et al., 2001) alleviates sample size reductions inherent in the categorical MATERIALS AND METHODS analysis and, although it does not identify fathers categorically, it Study species and study site provides an alternative way to estimate the distribution of mating P. canariensis is a diploid (n ¼ 18), long-lived, slow-growing, arborescent distances. Finally, spatially explicit mating models (Burczyk et al., monocot with a solitary trunk that grows up to B20 m, but most frequently 2002; Oddou-Muratorio et al., 2005) provide an inclusive tool to between 5 and 10 m. Numerous small yellowish male and female flowers jointly estimate the pollen dispersal kernel, pollen immigration rates cluster in spadices that develop on separate plants, being a dioecious species into the study area and phenotypic and ecological correlates of male with dimorphic flower and crown morphology traits. Flower anthesis happens at night or dawn and the flowering period lasts from few hours to 3 days in reproductive success. males and from 2 to 5 days in females, whereas fruit ripening takes 1 year after Phoenix canariensis Chabaud (Arecaceae) is an endemic and very fertilization. There is substantial flowering asynchrony between individuals representative palm species in the Canary Islands. Like all other within populations, being frequent to find at least some flowering individuals species belonging to the Canarian thermophilous woodland, Canarian through all the summer and autumn, that should facilitate outcrossing with palm populations suffered severe fragmentation after the Spanish palms from other groves. Although traditionally described as anemophilous, conquest and colonization in the fifteenth century because the fertile this pollination syndrome has been questioned because of male inflorescence areas that it inhabited were rapidly deforested for agriculture. traits and the presence of insects as flower visitors, both characters suggesting Thermophilous woodlands of the Canary islands grow preferentially entomophily pollination (Meekijjaroenroj and Anstett, 2003). Our recent between 300 and 500 m above sea level on windward wetter slopes, observations failed to detect any insect entering in female flowers, and and between 500 and 900 m on leeward drier slopes, as determined by therefore we favour the hypothesis that pollination is mainly by wind and that insects are just flower visitors (I Saro, unpublished data). the east–west distribution of the main mountain chains and the The study area was the Acusa Verde population, located on a leeward slope predominant northeastern trade winds (Ferna´ndez-Palacios and in northwestern Gran Canaria island (271 59.850 N, 151 41.330 O; at elevations Whittaker, 2008). The current natural distribution of P. canariensis from 505 to 686 m above sea level). This stand is one of the only four consists of palm groves that remain of a bygone wider natural populations registered as pure basic material for the collection of P. canariensis distribution, being mainly restricted to the bottom of ravines and forest reproductive material (BOE, 2006). It was chosen for its small size slopes with high moisture. It is most abundant in La Gomera and (B10 ha),
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