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Phylogeny and biogeography of Maclura (Moraceae) and the origin of an anachronistic fruit.
Mol Phylogenet Evol. 2017 12; 117:49-59.MP

Abstract

BACKGROUND AND AIMS

Maclura (ca. 12spp., Moraceae) is a widespread genus of trees and woody climbers found on five continents. Maclura pomifera, the Osage orange, is considered a classic example of an anachronistic fruit. Native to the central USA, the grapefruit-sized Osage oranges are unpalatable and have no known extant native dispersers, leading to speculation that the fruits were adapted to extinct megafauna. Our aim was to reconstruct the phylogeny, estimate divergence dates, and infer ancestral ranges of Maclura in order to test the monophyly of subgeneric classifications and to understand evolution and dispersal patterns in this globally distributed group.

METHODS

Employing Bayesian and maximum-likelihood methods, we reconstructed the Maclura phylogeny using two nuclear and five chloroplast loci from all Maclura species and outgroups representing all Moraceae tribes. We reconstructed ancestral ranges and syncarp sizes using a family level dated tree, and used Ornstein-Uhlenbeck models to test for significant changes in syncarp size in the Osage orange lineage.

KEY RESULTS

Our analyses support a monophyletic Maclura with a Paleocene crown. Subgeneric sections were monophyletic except for the geographically-disjunct Cardiogyne. There was strong support for current species delineations except in the widespread M. cochinchinensis. South America was reconstructed as the ancestral range for Maclura with subsequent colonization of Africa and the northern hemisphere. The clade containing M. pomifera likely diverged in the Oligocene, closely coinciding with crown divergence dates of the mammoth/mastodon and sloth clades that contain possible extinct dispersers. The best fitting model for syncarp size evolution indicated an increase in both syncarp size and the rate of syncarp size evolution in the Osage orange lineage.

CONCLUSIONS

We conclude that our findings are consistent with the hypothesis that M. pomifera was adapted to dispersal by extinct megafauna. In addition, we consider dispersal rather than vicariance to be most likely responsible for the present distribution of Maclura, as crown divergence post-dated the separation of Africa and South America. We propose revised sectional delimitations based on the phylogeny. This study represents a complete phylogenetic and biogeographic analysis of this globally distributed genus and provides a basis for future work, including a taxonomic revision.

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Authors+Show Affiliations

Gardner EM
Chicago Botanic Garden, Plant Science and Conservation, 1000 Lake Cook Road, Glencoe, IL 60022, USA; Northwestern University, Program in Plant Biology and Conservation, 2205 Tech Dr., Evanston, IL 60208, USA. Electronic address: egardner@u.northwestern.edu.
Sarraf P
Northwestern University, Program in Plant Biology and Conservation, 2205 Tech Dr., Evanston, IL 60208, USA.
Williams EW
Chicago Botanic Garden, Plant Science and Conservation, 1000 Lake Cook Road, Glencoe, IL 60022, USA.
Zerega NJC
Chicago Botanic Garden, Plant Science and Conservation, 1000 Lake Cook Road, Glencoe, IL 60022, USA; Northwestern University, Program in Plant Biology and Conservation, 2205 Tech Dr., Evanston, IL 60208, USA. Electronic address: n-zerega@northwestern.edu.

MeSH

AfricaBayes TheoremCell NucleusChloroplastsFruitGenes, PlantLikelihood FunctionsMacluraPhylogenyPhylogeographySouth America

Pub Type(s)

Journal Article

Language

eng

PubMed ID

28698111

Citation

Gardner, Elliot M., et al. "Phylogeny and Biogeography of Maclura (Moraceae) and the Origin of an Anachronistic Fruit." Molecular Phylogenetics and Evolution, vol. 117, 2017, pp. 49-59.
Gardner EM, Sarraf P, Williams EW, et al. Phylogeny and biogeography of Maclura (Moraceae) and the origin of an anachronistic fruit. Mol Phylogenet Evol. 2017;117:49-59.
Gardner, E. M., Sarraf, P., Williams, E. W., & Zerega, N. J. C. (2017). Phylogeny and biogeography of Maclura (Moraceae) and the origin of an anachronistic fruit. Molecular Phylogenetics and Evolution, 117, 49-59. https://doi.org/10.1016/j.ympev.2017.06.021
Gardner EM, et al. Phylogeny and Biogeography of Maclura (Moraceae) and the Origin of an Anachronistic Fruit. Mol Phylogenet Evol. 2017;117:49-59. PubMed PMID: 28698111.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Phylogeny and biogeography of Maclura (Moraceae) and the origin of an anachronistic fruit. AU - Gardner,Elliot M, AU - Sarraf,Paya, AU - Williams,Evelyn W, AU - Zerega,Nyree J C, Y1 - 2017/07/08/ PY - 2016/10/26/received PY - 2017/06/27/revised PY - 2017/06/29/accepted PY - 2017/7/13/pubmed PY - 2018/2/14/medline PY - 2017/7/13/entrez KW - Anachronistic fruit KW - Historical biogeography KW - Maclura KW - Megafauna dispersal KW - Moraceae KW - Osage orange SP - 49 EP - 59 JF - Molecular phylogenetics and evolution JO - Mol Phylogenet Evol VL - 117 N2 - BACKGROUND AND AIMS: Maclura (ca. 12spp., Moraceae) is a widespread genus of trees and woody climbers found on five continents. Maclura pomifera, the Osage orange, is considered a classic example of an anachronistic fruit. Native to the central USA, the grapefruit-sized Osage oranges are unpalatable and have no known extant native dispersers, leading to speculation that the fruits were adapted to extinct megafauna. Our aim was to reconstruct the phylogeny, estimate divergence dates, and infer ancestral ranges of Maclura in order to test the monophyly of subgeneric classifications and to understand evolution and dispersal patterns in this globally distributed group. METHODS: Employing Bayesian and maximum-likelihood methods, we reconstructed the Maclura phylogeny using two nuclear and five chloroplast loci from all Maclura species and outgroups representing all Moraceae tribes. We reconstructed ancestral ranges and syncarp sizes using a family level dated tree, and used Ornstein-Uhlenbeck models to test for significant changes in syncarp size in the Osage orange lineage. KEY RESULTS: Our analyses support a monophyletic Maclura with a Paleocene crown. Subgeneric sections were monophyletic except for the geographically-disjunct Cardiogyne. There was strong support for current species delineations except in the widespread M. cochinchinensis. South America was reconstructed as the ancestral range for Maclura with subsequent colonization of Africa and the northern hemisphere. The clade containing M. pomifera likely diverged in the Oligocene, closely coinciding with crown divergence dates of the mammoth/mastodon and sloth clades that contain possible extinct dispersers. The best fitting model for syncarp size evolution indicated an increase in both syncarp size and the rate of syncarp size evolution in the Osage orange lineage. CONCLUSIONS: We conclude that our findings are consistent with the hypothesis that M. pomifera was adapted to dispersal by extinct megafauna. In addition, we consider dispersal rather than vicariance to be most likely responsible for the present distribution of Maclura, as crown divergence post-dated the separation of Africa and South America. We propose revised sectional delimitations based on the phylogeny. This study represents a complete phylogenetic and biogeographic analysis of this globally distributed genus and provides a basis for future work, including a taxonomic revision. SN - 1095-9513 UR - https://www.unboundmedicine.com/medline/citation/28698111/Phylogeny_and_biogeography_of_Maclura__Moraceae__and_the_origin_of_an_anachronistic_fruit_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S1055-7903(17)30485-2 DB - PRIME DP - Unbound Medicine ER -