When species trees collide: phylogeny and historical biogeography of the cocosoid palms (Arecaceae, Arecoideae, Cocoseae) inferred from sequences of six WRKY gene family loci

Authors: Meerow, Alan; NOBLICK, LARRY - Montgomery Botanical Center; SALAS-LEIVA, DAYANA - Florida International University; Sanchez, Vanessa; FRANCISCO-ORTEGA, JAVIER - Florida International University; JESTROW, BRETT - Fairchild Tropical Botanic Garden; Nakamura, Kyoko

Submitted to: Cladistics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/9/2014
Publication Date: 1/4/2015
Citation: Meerow, A.W., Noblick, L., Salas-Leiva, D.E., Sanchez, V., Francisco-Ortega, J., Jestrow, B., Nakamura, K. 2015. When species trees collide: phylogeny and historical biogeography of the cocosoid palms (Arecaceae, Arecoideae, Cocoseae) inferred from sequences of six WRKY gene family loci. Cladistics. DOI: 10.1111/cla.12100.

Interpretive Summary: The coconut tribe (Cocoseae) is the most economically important natural group of palms, and includes oil palm, and peach palm as well as the coconut. It is most diverse in the American tropics with one and two genera found only in South Africa and Madagascar, respectively. The tribe is split into three subgroups, the coconut group, the oil palm group and the peach palm group. We used DNA sequences of six single copy genes to construct a tree of life of the whole tribe across 96 samples representing all of the genera and the two most closely related tribes. We analyzed the sequence matrix with a variety of analytical approaches that included combining all six genes together in a supermatrix, as well as using newer "species tree" estimation programs that evaluate each of the individual gene trees to develop a consensus. Congruent and well-resolved trees of life were obtained with the supermatrix. Those topologies differ slightly from a previous analysis with WRKY loci of only the coconut subgroup. It appears from these new analyses that the genus Attalea is most closely related to the coconus, Cocos nucifera. The resolution of the peach palm subgroup is best supported as being composed of two sister groups, the genera Bactris and Desmoncus in one, for which there is good supporting evidence from flower characters, and a second comprising the genera Acrocomia, Astrocaryum and Aiphanes. The biogeographic history of the coconut tribe is dominated by dispersal events. The tribe originated in the late Cretaceous, probably in northern South America and/or Central America, and dispersed throughout the Amazon region by the Paleocene. While the coconut subgroup disappeared from Central America, this region figured importantly in the early history of the other two subgroups, the oil palm and peach palm subtribes. Most the of the modern lineages in the entire tribe date to the Eocene. Eastern Brazil was the ancestral area for the American genera of the coconut subtribe. Several early lineages of the American coconut subtribe spread west to the proto-Andes and Chile, with subsequent isolation due to marine incursions and uplift of the Andean chain. The subtribe didn't reach Madagascar until the Eocene, which may represent migration through Cenozoic tropical Antarctica. Major lineages of the peach palm group evolved in the late Eocene, dispersing from Central America and Western Amazonas throughout the Amazon region, Northern South America and north to Mexico and the West Indies. Establishment of the major lineages of this group appear contemporary with the terminal Eocene cooling event. The presence of Elaeis in Africa dates to the late Miocene and appears to be a long-distance dispersal event. Evaluated together, the supermatrix and species tree analyses presented in this paper give us the most accurate picture of the evolutionary history of the tribe to date, with more congruence than incongruence among the various methodologies.

Technical Abstract: Arecaceae tribe Cocoseae is the most economically important tribe of palms, wherein both coconut and African oil palm are classified. It is mostly represented in the Neotropics, with one and two genera endemic to South Africa and Madagascar, respectively. Three subtribes are recognized: Attaleinae, Bactridinae and Elaeidinae. Using primers designed from six single copy WRKY gene family loci isolated from Cocos nucifera, we amplified DNA from 96 samples representing all genera of the palm tribe Cocoseae as well as from outgroup taxa representing tribes Roystoneae and Reinhardtieae. We compared the parsimony (MP), maximum likelihood (ML), and Bayesian (B) analysis of the supermatrix with three species tree estimation approaches. Congruent and well-resolved topologies from MP and ML analyses were obtained with the supermatrix. Those topologies differ slightly from a previous analysis with WRKY loci of only subtribe Attaleinae with one species each of Elaeis and Bactris as outgroup. B analysis, also well-resolved, is discordant with MP and ML at two nodes. Lytocaryum, previously nested in Syagrus, is now positioned by MP and ML as sister to the former with high support; B analysis maintains Lytocaryum embedded within Syagrus. MP and ML resolve Cocos as sister to Syagrus; B positions Cocos as sister to Attalea. Most strikingly, two small sister clades with an Andean/Eastern Brazilian disjunct are now the first branches in the American endemic Attaleinae with a consequent more ancient age estimation at their stem nodes. Subtribe Elaeidinae is sister to the Bactridinae in all analyses. The resolution of genera of Bactridineae varies as well, but is best supported as being composed of two sister clades, Bactris and Desmoncus in one, for which there is morphological evidence as well, and a second comprising Acrocomia, Astrocaryum and Aiphanes. Two B gene tree-species estimation approaches are incongruent with the supermatrix in a few critical intergeneric clades, but resolve the same infrageneric relationships. Both position Cocos as sister to Attalea, albeit with low support. If this is applied as a constraint on the supermatrix MP analysis, it results in trees only 4 steps longer. The biogeographic history of the Cocoseae is dominated by dispersal events. The tribe originated in the late Cretaceous, probably in northern South America and/or Central America, and dispersed throughout the Amazon region by the Paleocene. The Attaleinae were extirpated from Central America, while this region figured importantly in the early history of the other two subtribes. Divergence of Elaeidinae and Bactridinae dates to the early Eocene. Major lineages of Bactridinae evolved in the late Eocene, dispersing from Central America and Western Amazonas throughout the Amazon region, Northern South America and north to Mexico and the West Indies. The Attaleinae diverged from the other two subtribes in the early Paleocene, with modern lineages not originating until the late Eocene in Eastern Brazil. Establishment of the major clades of American Attaleinae occured during the Oligocene and Miocene. The subtribe is mostly absent from Central America, except for the broadly distributed Cocos nucifera, and some Attalea species that dispersed in the late Neogene. Several early lineages of the American Attaleinae spread west to the proto-Andes and Chile, with subsequent vicariance, perhaps due to marine incursions and uplift of the Andean chain. The subtribe didn't reach Madagascar until the Eocene, which may represent migration through Cenozoic tropical Antarctica. Establishment of the major clades of Bactridinae appears congruent with the terminal Eocene cooling event. The presence of Elaeis in Africa dates to the late Miocene and appears to be a long-distance dispersal event. Evaluated together, the supermatrix and species tree analyses