Admixture may be extensive among hyperdominant Amazon rainforest tree species

Abstract

Admixture is a mechanism by which species of long-lived plants may acquire novel alleles. However, the potential role of admixture in the origin and maintenance of tropical plant diversity is unclear. We ask whether admixture occurs in an ecologically important clade of Eschweilera (Parvifolia clade, Lecythidaceae), which includes some of the most widespread and abundant tree species in Amazonian forests. Using target capture sequencing, we conducted a detailed phylogenomic investigation of 33 species in the Parvifolia clade and investigated specific hypotheses of admixture within a robust phylogenetic framework. We found strong evidence of admixture among three ecologically dominant species, E. coriacea, E. wachenheimii and E. parviflora, but a lack of evidence for admixture among other lineages. Accepted species were largely distinguishable from one another, as was geographic structure within species. We show that hybridization may play a role in the evolution of the most widespread and ecologically variable Amazonian tree species. While admixture occurs among some species of Eschweilera, it has not led to widespread erosion of most species' genetic or morphological identities. Therefore, current morphological based species circumscriptions appear to provide a useful characterization of the clade's lineage diversity.

Keywords: Amazon basin; Lecythidaceae (Brazil nut family); Parvifolia clade; adaptive introgression; hybridization; hyperdominance; target enrichment sequencing; tropical diversity.

Fig. 1

Examples of the morphology of members of the Parvifolia clade. (a) Flower of Eschweilera parviflora. (b) Lateral view of a flower of Eschweilera wachenheimii. (c) Flower of Eschweilera coriacea. (d) Flower of Eschweilera collina with androecial hood sectioned. (e) Fruit bases, opercula and seeds of Eschweilera parviflora. (f) Fruits, operculum and seeds of Eschweilera coriacea. (g) Leaves and old fruit of Eschweilera atropetiolata. (h) Abaxial view of a leaf of Eschweilera coriacea. (i) Bark of Eschweilera tessmannii. (j) Bark of Eschweilera truncata. (k) Bark of Eschweilera sagotiana. (l) Bark of Eschweilera atropetiolata. Photograph attribution: (a, b, e, f, g, i, j, l) to Scott Alan Mori; (c, d, k) to Carol Ann Gracie; (h) to Xavier Cornejo. Reproduced under terms of the CC BY‐NC‐SA 3.0 license. Captions are adapted from Mori et al. ( onward).

Fig. 2

Schematic of the rooted triplet test for assessing evidence of admixture. Red arrows indicate four hypothetical samples selected for the test. The test assumes that the outgroup diverges first in all gene trees and at least two species are represented in the ingroup. Blue and red phylogenies represent the two possible topologies that conflict with the most common topology after all possible gene trees have been generated. Any statistically significant deviation from equal numbers of the two conflicting topologies, where P is the probability of a result at least as unequal as the observed frequencies using a binomial test, is considered evidence that the assumptions of the multispecies coalescent have been violated by admixture among species.

Fig. 3

Population structure (K = 5) of all samples in the clade that included E. coriacea, E. wachenheimii, E. truncata and E. parviflora. Each bar represents the ancestry of an individual inferred with structure. Each individual is labelled with a unique code used throughout all analyses and asterisks indicate samples from focal species collected at Reserve 1501. Collection locations outside Reserve 1501 are indicated as follows: Pa – Panama, Pe – Peru, E – Ecuador, F – French Guiana, B – Brazil. Black stars above bars indicate individuals with significant evidence of admixture based on an RT test.

Fig. 4

Phylogeny of the Parvifolia clade visualized using a single representative per accepted species. Branch labels are iq‐tree ultrafast bootstrap support. Asterisks on branch labels indicate relationships that conflict with the best‐scoring maximum likelihood topology recovered with an exon‐only supermatrix. The results of structure analyses are shown for SNP datasets that included all individuals within the corresponding clades indicated on the phylogeny. Each individual is labelled with a unique code used throughout all analyses and asterisks on these labels indicate samples from focal species collected at Reserve 1501. The legend for each subplot indicates the one or more species that most closely corresponded to each cluster based on accepted taxonomy. The individuals in these clades generally clustered along morphologically defined species boundaries and there was no significant evidence of admixture for these taxa based on rooted triplet tests.

Fig. 5

Occurrence records across the Neotropics for four closely related species in the Parvifolia clade, three of which show evidence of admixture in this study. Few or no records are available for these species across much of the Amazon basin as most come from collections made in permanent plots. Because of this, there is uncertainty regarding the true extent of range overlap among these and other species of Lecythidaceae as is the case for many other clades of Neotropical trees.