Seed dispersal by animals: exact identification of source trees with endocarp DNA microsatellites

Abstract

A long-standing challenge in studies of seed dispersal by animal frugivores has been the characterization of the spatial relationships between dispersed seeds and the maternal plants, i.e. the seed shadow. The difficulties to track unambiguously the origin of frugivore-dispersed seeds in natural communities has been considered an unavoidable limitation of the research field and precluded a robust analysis of the direct consequences of zoochory. Here we report that the multilocus genotype at simple sequence repeat (SSR; microsatellite) loci of the woody endocarp, a tissue of maternal origin, provides an unequivocal genetic fingerprint of the source tree. By comparing the endocarp genotype against the complete set of genotypes of reproductive trees in the population, we could unambiguously identify the source tree for 82.1% of the seeds collected in seed traps and hypothesize that the remaining 17.9% of sampled seeds come from other populations. Identification of the source tree for Prunus mahaleb seeds dispersed by frugivores revealed a marked heterogeneity in the genetic composition of the seed rain in different microhabitats, with a range of 1-5 distinct maternal trees contributing seeds to a particular landscape patch. Within-population dispersal distances ranged between 0 and 316 m, with up to 62% of the seeds delivered within 15 m of the source trees. Long distance dispersal events, detected by the exclusion of all reproductive trees in the population, accounted for up to 17.9% of the seeds sampled. Our results indicate strong distance limitation of seed delivery combined with infrequent long-distance dispersal events, extreme heterogeneity in the landscape pattern of genetic makeup, and a marked mosaic of multiple parentage for the seeds delivered to a particular patch.

Spatial genetic structure of Simarouba amara Aubl. (Simaroubaceae), a dioecious, animal-dispersed Neotropical tree, on Barro Colorado Island, Panama

“…Current modeling techniques, however, likely underestimate seed dispersal distances because they assume seeds in traps arrive from the nearest adult tree. Models also fail to adequately account for long-distance seed input that may play a substantial role in spatial genetic processes (Oddou-Muratorio et al, 2001), as well as individual variability in fecundity and survivorship (Godoy and Jordano, 2001). Perhaps most importantly for the present study, the current models fail to incorporate dioecy and thus underestimate seed dispersal because any reproductive size adult is considered a potential seed donor.…”

Distribution and fine-scale spatial-genetic structure in British wild cherry (Prunus avium L.)

“…This suggests that populations A and B were established by similar founding material and that subsequent geneflow into the two populations has been similar. Previous work in P. mahaleb indicated that the majority of seed dispersed beneath a maternal tree were its own progeny with up to 62% of seeds being delivered within 15 m of the source tree (Godoy and Jordano, 2001). Earlier studies in wild cherry also noted that the vast majority of wild cherry seed was dispersed no further than 50 m from the mother tree (Turcek, 1968).…”

“…However, in a Slovakian wild cherry population, isoenzyme polymorphism did reveal significant levels of SGS in the first distance class examined (o36.8 m) (Gö mö ry and Paule, 2001). Microsatellite or simple sequence repeat (SSR) markers are codominant and highly polymorphic and have been widely used in forest tree population studies over recent years (Godoy and Jordano, 2001;Asuka et al, 2004;Heuertz et al, 2004;Marquardt and Epperson, 2004). Recently, we have optimized a suite of SSR markers from P. avium to enable the efficient genotyping of wild cherry in population scale studies (Vaughan and Russell, 2004).…”

Geographic consistency in the seed dispersal patterns of Taxus baccata L. in the Iberian Peninsula

“…In temperate ecosystems, the main seed dispersers of fleshy-fruited trees are carnivorous mammals and birds (Guitián & Munilla, 2010;García et al, 2010;Peredo et al, 2013). Birds typically account for a large proportion of dispersed seeds (Jordano, 1987;Herrera, 1998;Martínez et al, 2008), depositing them at very short distances from mother trees (Godoy & Jordano, 2001;Jordano et al, 2007;Martínez et al, 2008), and usually under tree canopies as a result of their active selection of forest habitats (Alcántara et al, 2000;Jordano & Schupp, 2000;Martínez et al, 2008;Martínez & García, 2015a). This is the case of yew in the Cantabrian mountains (N Spain), for which birds tend to disproportionately disperse the seeds beneath conspecific adult trees (García et al, 2005b;Martínez et al, 2008), a pattern that may hamper recruitment due to increase predation, pathogen attack, and competition in high-density seed or seedling clumps (JanzenConnell effects;Janzen, 1970;Schupp & Jordano, 2011;Devaney et al, 2014).…”