Contrasting demographic history and population structure of Zamia (Cycadales: Zamiaceae) on five islands of the Greater Antilles suggests a model for population diversification in the Caribbean clade of the genus

Authors: Meerow, Alan; SALAS-LEIVA, DAYANA - Florida International University; CALONJE, MICHAEL - Montgomery Botanical Center; ORTEGA, JAVIER - Florida International University; GRIFFITH, M. PATRICK - Montgomery Botanical Center; Nakamura, Kyoko; JIMENEZ-RODRIGUEZ, FRANCISCO - National Botanical Garden; LAWRUS, JOHN - Queen Elizabeth Ii Botanic Park; OBERLI, ANDREAS - Non ARS Employee

Submitted to: International Journal of Plant Sciences
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/13/2018
Publication Date: 11/1/2018
Citation: Meerow, A.W., Salas-Leiva, D., Calonje, M., Ortega, J.F., Griffith, M., Nakamura, K., Jimenez-Rodriguez, F., Lawrus, J., Oberli, A. 2018. Contrasting demographic history and population structure of Zamia (Cycadales: Zamiaceae) on five islands of the Greater Antilles suggests a model for population diversification in the Caribbean clade of the genus. International Journal of Plant Sciences. 179:730-757.

Interpretive Summary: The three largest islands of the Greater Antilles after Cuba are Hispaniola, Jamaica (JAM), and Puerto Rico (PR), all of which are inhabited by the Zamia pumila complex, a group of cycads distributed through the Greater Antilles, the Bahamas and Florida, and very popular landscape ornamentals. In this paper, we used 21-28 nuclear DNA repeat markers and 10 single copy nuclear genes, to understand the patterns of genetic variation that occur throughout 30 populations of the complex in CAY, the Dominican Republic (DR), JAM and PR. The two DNA marker systems have very different mutation rates, thus each captures a different time scale in the history of these populations. We found that each island exhibits a different patterns of genetic variation, gene flow, and migration. DR and PR evolved from a common ancestral gene pool. The large populations in DR show high levels of inter-breeding and very low differentiation. PR fits a model of semi-speciation. Northern and western populations in JAM represent separate introductions to the island. Overall, JAM shows minimal levels of gene flow among populations, and has exchanged genes with CAY, perhaps as a consequence of human introduction. Niche adaptation and associated morphological character states evolve in parallel among different islands in response to environmental and other variables. We present a model of how these plants diversified in the Greater Antilles.

Technical Abstract: After Cuba, the three largest islands of the Greater Antilles are Hispaniola, Jamaica (JAM), and Puerto Rico (PR), all of which are inhabited by the Zamia pumila complex, a monophyletic group of dioecious gymnosperms treated as a single polymorphic or as many as nine species. We sought to test the following hypotheses for Zamia: (i) Dominican Republic (DR) and JAM fit evolutionary models of panmixis and isolation, respectively; (ii) historical gene flow has occurred between PR and DR, and admixture between the Caymans (CAY) and JAM; and (iii) vegetative morphological characters in common to populations on different islands do not conform to genetic relationships. We genotyped a total of 30 populations from CAY, DR, JAM and PR with 21-28 microsatellite loci (SSRs), and haplotypes from ten single copy nuclear genes (SCNGs), and analyzed the data with permuted AMOVA, Bayesian clustering, ABC coalescent modeling, network, and gene flow analyses. By using two different sets of molecular markers with very different mutation rates (SSR and SCNGs), we sought to capture two distinct time slices of evolutionary history in the populations of each island. Diversification of Caribbean Zamia follows a different path on each island after migration or vicariance from ancestors putatively originating in Cuba. DR and PR evolved from a common ancestral gene pool. DR fits a model of panmixis, while PR fits a vicariance model of semi-speciation. Northern and western populations in JAM represent separate introductions to the island. Overall, JAM shows minimal levels of gene flow among populations, and apparent admixture with CAY. We conclude that niche adaptation and associated vegetative morphological character states evolve convergently among different islands in response to environmental and other stochastic variables. We present a model of how these dioecious gymnosperms diversified in the Greater Antilles.