The importance of environmental heterogeneity and spatial distance in generating phylogeographic structure in edaphic specialist and generalist tree species of Protium (Burseraceae) across the Amazon Basin

Abstract

Aim Edaphic heterogeneity may be an important driver of population differentiation in the Amazon but remains to be investigated in trees. We compared the phylogeographic structure across the geographic distribution of two Protium (Burseraceae) species with different degrees of edaphic specialization: Protium alvarezianum, an edaphic specialist of white‐sand habitat islands; and Protium subserratum, an edaphic generalist found in white sand as well as in more widespread soil types. We predicted that in the edaphic specialist, geographic distance would structure populations more strongly than in the edaphic generalist, and that soil type would not structure populations in the edaphic generalist unless habitat acts as a barrier promoting population differentiation. Location Tropical rain forests of the Peruvian and Brazilian Amazon, Guyana and French Guiana. Methods We sequenced 1209–1211 bp of non‐coding nuclear ribosomal DNA (internal transcribed spacer and external transcribed spacer) and a neutral low‐copy nuclear gene (phytochrome C) from P. subserratum (n = 65, 10 populations) and P. alvarezianum (n = 19, three populations). We conducted a Bayesian phylogenetic analysis, constructed maximum parsimony haplotype networks and assessed population differentiation among groups (soil type or geographic locality) using analysis of molecular variance and spatial analysis of molecular variance. Results The edaphic specialist exhibited considerable genetic differentiation among geographically distant populations. The edaphic generalist showed significant genetic differentiation between the Guianan and Amazon Basin populations. Within Peru, soil type and not geographic distance explained most of the variation among populations. Non‐white‐sand populations in Peru exhibited lower haplotype/nucleotide diversity than white‐sand populations, were each other’s close relatives, and formed an unresolved clade derived from within the white‐sand populations. Main conclusions Geographic distance is a stronger driver of population differentiation in the edaphic specialist than in the generalist. However, this difference did not appear to be related to edaphic generalism per se as adjacent populations from both soil types in the edaphic generalist did not share many haplotypes. Populations of the edaphic generalist in white‐sand habitats exhibited high haplotype diversity and shared haplotypes with distant white‐sand habitat islands, indicating that they have either efficient long‐distance dispersal and/or larger ancestral effective population sizes and thus retain ancestral polymorphisms. These results highlight the importance of edaphic heterogeneity in promoting population differentiation in tropical trees.

Insect herbivores, chemical innovation, and the evolution of habitat specialization in Amazonian trees

“…(Left) A Bayesian phylogeny based on three nuclear genes of Protium subserratum populations from Fine et al (2013) showing white-sand ecotypes from Peru (white circles, triangles, and squares), terra firme ecotypes from Peru (gray circles, triangles, and squares), and terra firme ecotypes from Manaus Brazil (indicated with ''M''). First, we used generalized linear models and a negative binomial error structure to compare the number of insects and morphospecies observed per plant and the number of host plants on which morphospecies were collected with crossed predictors of habitat type and FIG.…”

“…Of these species, Protium subserratum Engl. Although there are consistent morphological differences that characterize the terra firme and white-sand ecotypes, there is also evidence of limited gene flow (or incomplete lineage sorting) between the two ecotypes (Fine et al 2013). comprises morphologically divergent ecotypes that correspond to white-sand and terra firme habitats, often occurring within meters of one another in a parapatric distribution Fine 2011, Fine et al 2013).…”

Habitat-specific divergence of procyanidins in Protium subserratum (Burseraceae)

“…3, 4). Interestingly, a phylogeographic study of Peruvian WS, BS, and CS ecotypes showed no variation in haplotypes between BS and CS individuals (Fine et al 2013b). Microsatellite studies are thought to reflect much more recent signals of population-level divergence than sequence data (Misiewicz and Fine 2014).…”

“…They are morphologically distinct and often occur within meters of each other in a parapatric distribution (Fine et al 2013a;Misiewicz and Fine 2014). Phylogeographic analyses of the haplotypes of these three morphotypes as well as detailed population genetic study have revealed that they represent three evolutionary lineages although there is limited gene flow among them (Fine et al 2013b;Misiewicz and Fine 2014). Thus, these ecotypes either represent recently derived species or lineages undergoing incipient speciation.…”

Plant Ontogeny, Spatial Distance, and Soil Type Influence Patterns of Relatedness in a Common Amazonian Tree

“…(Burseraceae) is a widespread species found in northern Amazonia, extending into Guyana, French Guyana, the Brazilian Amazon, Ecuador, Peru, Colombia and Venezuela. This dioecious tree species occurs across a range of soil types including clay, sandy clay and white sand [22] and its red fruits are thought to be dispersed by birds and monkeys [23]. We studied a population of P. subserratum along an edaphic and topographic gradient within the Reserva Florestal Adolpho Ducke (hereafter referred as Ducke), where this species is found across a soil gradient that transitions from sandy soil in low elevation areas (39 m a.s.l.)…”