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Article

Phylogeography of Coccoloba uvifera (Polygonaceae) Sampled across the Caribbean Basin

by
Danny J. Gustafson
1,*,
Logan A. Dix
1,
Derek P. Webster
1,
Benjamin K. Scott
1,
Isabella E. Gustafson
2,3,
Aidan D. Farrell
4 and
Daniel M. Koenemann
5
1
Department of Biology, The Citadel, Charleston, SC 29409, USA
2
Department of Biological Sciences, Marine Biology, University of South Carolina, Columbia, SC 29208, USA
3
Grice Marine Laboratory, College of Charleston, Charleston, SC 29412, USA
4
Department of Life Sciences, University of the West Indies, St. Augustine 685509, Trinidad and Tobago
5
Department of Education and Liberal Arts, Catholic International University, Charles Town, WV 25414, USA
*
Author to whom correspondence should be addressed.
Diversity 2024, 16(9), 562; https://doi.org/10.3390/d16090562 (registering DOI)
Submission received: 31 July 2024 / Revised: 2 September 2024 / Accepted: 5 September 2024 / Published: 8 September 2024
(This article belongs to the Section Biogeography and Macroecology)
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Abstract

:
Coccoloba uvifera L. (seagrape) is a primarily dioecious neotropical tree species which often grows in the beach–forest transitional ecotone of coastal strand vegetation. We used five maternally inherited non-coding chloroplast regions to characterize the phytogeography of C. uvifera collected across the Caribbean Basin and Florida. Bayesian analysis revealed divergence between the Aruba–Trinidad–Tobago–Antigua–Jamaica island group and the continental Belize–Florida–US Virgin Islands (USVI) group at 1.78 million years before present (mybp), divergence between the Belize and Florida–USVI groups at 1.08 mybp, and a split of Antigua–Jamaica from Aruba–Trinidad–Tobago at 0.217 mybp. Haplotype network analysis supports the three clades, with the island group possessing the oldest haplotype. Based on geology and proximity, these clades correspond to South American (oldest), Central American, and North American (most recent). Coccoloba uvifera demographic expansion occurred during the Pleistocene epoch and peaked near the end of the last glacial maximum (ca. 0.026–0.019 mybp) when the global sea levels were 125 m lower than today. Our findings also reveal that tropical cyclones, which often impact coastal strand vegetation, did not affect genetic diversity. However, there was a positive association between latitude and the average number of substitutions, further enriching our understanding of the species’ phytogeography.

1. Introduction

Coccoloba uvifera (L.) is an indigenous tropical and subtropical American genus with 120–150 species and one of a few tropical genera in the Polygonaceae family. Coccoloba uvifera is a significant vegetative component of coastal strand habitats along the Atlantic, Caribbean, and Pacific coasts of the American tropics and subtropics between 25N and 10S latitudes [1,2]. This woody species typically grows at the transition between beach and forest [2,3]. It protects beach habitats during tropical storms and hurricanes, serving as an essential habitat and animal food source [2,4]. While often considered primarily dioecious [2,3], Madriz and Ramirez [5] documented polygamo-dioecy in a Venezuelan population with 22% monecious individuals who were self-compatible but with a reduced fruit and seed set relative to dioecious plants. Most species (85) are South American, with C. uvifera and C. diversifolia (Jacq.) reaching their northern limit in Florida [6].
North America separated from Laurasia, and South America separated from Gondwana during the Jurassic–Cretaceous periods (200 to 145 mybp). The Greater Antilles (Cuba, Hispaniola, Puerto Rico, Jamaica, Cayman Islands, and geologically the Virgin Islands) predate the Isthmus of Panama and the volcanic origin of the Lesser Antilles Islands (3 to 3.5 mybp) [7]. Fossil leaves and pollen records suggest the origin of the genus Coccoloba is North American [6,8,9,10], which is supported by the only molecular phylogeny of the genus [11]. Alternately, a South American origin for Coccoloba has been suggested based on extensive early taxonomic work by Howard [12] and the more recent molecular systematics work of Schuster et al. with Coccoloba as part of the Eriogonoideae [13].
As C. uvifera occurs in the strand habitat within the Caribbean Basin, tropical storms and hurricanes likely influence its survival and dispersal. Tropical hurricanes are unavoidable, large-scale disturbances that significantly affect natural ecosystems and human societies. The frequency, size, and intensity of these weather events can influence the structure of tropical forests [14,15,16]. Wind damage during hurricanes can cause significant reductions in canopy cover through defoliation and tree mortality, encourage higher regeneration and biomass turnover, and create opportunities to recruit subdominant tree species [17,18,19,20,21]. A higher demographic turnover in storm-impacted populations could influence genetic diversity within the population of C. uvifera. In addition to wind damage, physiological salt stress and physical damage from storm surges are a significant concern for species at low elevations in coastal areas [22,23]. At the same time, the distribution of hurricanes in time and space is not uniform across the Caribbean Basin. For example, the island of Aruba has experienced zero major hurricanes (Cat. 3-5) since 1842, while the island of Antigua has experienced 13 major hurricanes in the same period (https://coast.noaa.gov/hurricanes/ (accessed on 12 June 2024)). Ecological disturbance has been shown to influence genetic diversity [24,25,26,27]. Therefore, it may be possible to identify differences in C. uvifera genetic diversity as a function of site hurricane history.
In this molecular phylogeography study, we use five non-coding chloroplast regions to assess historical biogeographic processes and disturbance dynamics on the spatial genetic structure of Coccoloba uvifera sampled across the neotropics. The genetics of C. uvifera are complicated by unresolved phylogenetic relationships within the genus [11], the complex ploidy level (2n = 132), and the potential for hybridization with closely related species [6]. In flowering plants, chloroplast and mitochondrial DNA are usually maternally inherited; therefore, the genetic structure based on organelle DNA is a record of seed dispersal history [28,29]. In this study, we use non-coding chloroplast regions to characterize the haploid distribution of C. uvifera across the Caribbean Basin (Figure 1). Non-coding chloroplast regions were selected for this study because of the maternal inheritance; they are not affected by polyploidy, and the spatial genetic pattern will reflect the seed dispersal dynamics of this animal-dispersed (zoochory) seagrape fruit [30,31]. This intraspecific biogeography study aims to determine (a) the biogeographic genetic pattern across the Caribbean Basin, (b) whether C. uvifera originated from North America or South America, and (c) if spatial–temporal variation in hurricanes affect genetic diversity.

2. Materials and Methods

2.1. Sampling and Lab Procedures

We collected leaves from five to seven plants separated by at least two meters and recorded GPS coordinates from nine locations across the Caribbean Basin and Florida, U.S.A. (Figure 1, Table S1). Leaves were rinsed in diH2O, dried on silica gel, and then stored at −20 °C until extracted. The EZNA Plant DNA Kit was used to extract total genomic DNA (Omega Bio-tek, Inc., 400 Pinnacle Way, Suite 450, Norcross, GA, USA) using a liquid nitrogen DNA extraction procedure adopted from Gustafson et al. [32] and modified for the high-lignin-content leaves. We surveyed nine fast-evolving chloroplast gene regions identified in Shaw et al. [31], selected five for this study, and then designed specific primers for C. uvifera (Table 1). The chloroplast genome, also known as the plastome, is a single circular molecule of double-stranded DNA organized into a large single-copy region, two inverted repeats, and a small single-copy region. Three gene regions are located in the large single-copy region and two in the more variable small single-copy region [33]. All PCR reactions were 25 μL reactions consisting of 12.5 μL Master Mix, 1 μL each primer at 10 μM, 10 μL molecular-grade dH2O, and 1 μL DNA template. A Bio-Rad MJ-mini (PTC-1148) Thermocycler (Bio-Rad, Hercules, CA, USA) was used with the following thermocycling conditions: an initial denaturation of 95 °C for 4 min, followed by 29 cycles of 95 °C for 1 min, 61 °C for 1 min, and 72 °C for 1 min, followed by a final extension of 72 °C for 4 min. We verified successful amplifications by running PCR products on a 1% agarose gel stained with ethidium bromide. PCR products were cleaned using the E.Z.N.A. Cycle Pure Kit (Omega Bio-tek, Inc., 400 Pinnacle Way, Suite 450, Norcross, GA), and then submitted for Sanger sequencing by Eton Bioscience (Eton Bioscience, 400 Park Offices Dr., Research Triangle Park, North Carolina 27709). A standard sequencing protocol was used for all sequences except forward primer C (ndhA intron), which required special sequencing conditions for complex templates.

2.2. Sequence Alignment

The DNA sequences were aligned, inspected, and manually adjusted using ClustalW for each of the five loci (ChromasPro ver. 2.1.8, Technelysium Pty Ltd., 8 Cordelia St., South Brisbane, Australia). Gaps were coded using simple indel coding [34] and implemented in SeqState 1.4.1 [35]. We included 15 indels, which did not represent autapomorphies. Indel mutations were coded as binary characters and appended to the sequence data matrix for haplotype network analyses.

2.3. Genetic Structure and Genetic Diversity

To assess population structure, we conducted an analysis of molecular variance (AMOVA) based on haplotype frequencies, with significance tested by 10,200 permutations. Fu’s Fs test of selective neutrality was used to test the hypothesis of selective neutrality and population equilibrium using a coalescent simulation algorithm. Diversity, neutrality, and population structure analyses were performed using the software Arlequin 3.5.2.2 [36]. The total number of tropical cyclones (Tropical Storm Category 5) and major hurricanes (Category 3-5) passing within 60 miles of the location between 1842 and 2021 was generated using Historical Hurricane Tracks, an interactive mapping tool that uses the NOAA National Hurricane Center HURDAT2 and NOAA National Centers for Environmental Information IBTrACS data sets (https://coast.noaa.gov/hurricanes (accessed on 12 June 2024)). Pearson Correlation analysis was used to test for associations between genetic measure and latitude with the number of tropical storms and hurricanes (TS-Cat. 5), as well as major hurricanes (Cat. 3-5), that passed within 60 nautical miles of the sites between 1842 and 2021 (SigmaPlot 14.0, Systat Software Inc., Palo Alto, CA, USA) (Table S2).

2.4. Evolutionary Relations and Time of Divergence between Haplotypes

We inferred the haplotype network using statistical parsimony analysis to estimate gene genealogies using TCS 1.13 [37] in PopART v.1.7 [38]. This haplotype network method produced a network of both sampled and unsampled intermediate haplotypes. Haplotypes in the network were joined at a 95% significance level.
Spherical phylogeography coalescent analysis, using the GEO_SPHERE package in BEAST [39], was used to infer the historical phylogeography of GPS-referenced C. uvifera individuals based on the five chloroplast regions. This Bayesian phylogeography method based on diffusion on a sphere removes distortion introduced by map projections, like the Mercator projection. Using point coordinates allows for incorporating uncertainties in all the model parameters, integrated time trees, and biogeographic inference. We specified the Bayesian analyses with BEAUti v2.6.7 [40]. The five regions were partitioned separately, the nucleotide substitution model-averaging method (bModelTest tool; [41]) assigned the BEAST Model Test averaging substitution model, and the strict clock model rate was set to the published non-coding chloroplast gene substitution mutation rate (1.52*10−9 nucleotides/site/year; [42]). The geographic partition was assigned an uncorrelated log-normal clock with a mean rate of 1.0 and estimated. We inferred trees under the coalescent constant population model. Four independent analyses were run for 100 million generations each, sampling every 5000th generation and discarding the first 25% as burn-in. We assessed the parameters for each independent run using Tracer v1.7.1 [43]. LogCombiner v2.6.7 combined the four independent runs with sampling every 10,000 generations for the log and tree files. A maximum clade credibility tree was annotated, and diffusion estimates were generated using TreeAnnotator v2.6.0 after discarding 25% of the trees as burn-in, then visualized in FigTree v1.4.4 (http://tree.bio.ed.ac.uk/software/figtree/ (accessed on 1 January 2020)).
We investigated the demographic dynamics using a coalescence Bayesian Skyline Plot (BSP) [44]. We used the same characteristics of the Spherical Phylogeography Coalescent Analysis, except the trees were inferred under the Bayesian Skyline model and displayed as skyline plots [43].

3. Results

We identified 26 haplotypes for the 51 C. uvifera plants sampled from the survey of nine populations across the Caribbean Basin and Florida (Figure 1). Nine haplotypes (H1-H9) were shared between two to three populations, while the remaining 17 haplotypes were unique. Each population contained two to seven haplotypes, with no shared haplotypes within the Florida, St. John, and St. Croix populations (i.e., Florida-USVI) (Table 2). The three Florida–USVI populations also had the highest number of private substitution sites. Nucleotide diversity and the mean number of pairwise differences covary, with St. Croix having the highest and Antigua having the lowest diversity estimates. We did not observe significant deviations from neutrality for any population based on Fu’s Fs test of selective neutrality. The analysis of molecular variance (AMOVA) showed a significant proportion (ϕST = 0.5393, p < 0.0001) of the total variance explained by differences among populations (Table 3).
The TCS haplotype maximum parsimony network revealed 26 haplotypes separated into three groups: an ‘Island group’ (Aruba–Trinidad–Tobago–Antigua–Jamaica), a ‘Central American group’ (Belize), and a ‘North American group’ (Florida–USVI) (Figure 2). The oldest probable haplotype, H01, stands out as the most common and geographically widespread across the islands of Aruba, Trinidad, Tobago, Antigua, and Jamaica. It forms the core of the star gene tree pattern and is one mutational step away from seven of the ten haplotypes. Five of the seven H01-associated haplotypes are shared between individuals from the same population (H05 and H07) or among different populations (H03, H06, and H08). The Belize group is separated from the Island group by 14 mutations and contains the second most common haplotype (H02). The centrally located Belize group is separated from the Florida–USVI group by 11 mutations. Notably, one haplotype (H04) was shared among two plants from Aruba and one from St. John, while all other haplotypes in this Florida, St. Johns, and St. Croix group are unique.
The phylogeographic relationships were elucidated using five non-coding chloroplast C. uvifera regions and BEAST spherical phylogeography coalescent analysis. The results clearly showed divergence of the Island group from the Central American (Belize) and North American (FL-USVI) groups, which occurred at approximately 1.78 mybp (95% highest posterior density (HPD) 2.62–1.03 mybp) (Figure 3). The next oldest divergence is between the Central American (Belize) and North American (Florida–USVI) groups, which occurred at around 1.08 mybp (95% HPD 1.61–0.58 mybp). Within the Island group, the Antilles islands of Antigua and Jamaica diverged from the South American-associated islands of Aruba, Trinidad, and Tobago by approximately 0.217 mybp (95% HPD 0.379–0.090 mybp).
The coalescent Bayesian Skyline Plot analysis showed a demographic expansion of C. uvifera starting around 324,000 years before the present and peaking near the end of the global last glacial maximum (Figure 4). This demographic expansion coincides with the divergence of the Aruba, Trinidad, and Tobago island populations from the Antigua and Jamaica island populations at 0.217 mybp (95% HPD 0.379–0.090 mybp). The increased variance in population estimates at the most recent (tip-ward) end of the skyline plot is likely a result of limited sequence variation and the small coalescent intervals in the estimated trees [44].
The total number of tropical cyclones (TS-Cat. 5) was positively correlated with latitude and the number of major (Cat. 3-5) hurricanes (Table 4). The mean number of substitutions, transitions, and transversions were all correlated with each other, along with nucleotide diversity and pairwise differences, but not with the haplotype number (Table 4). Latitude was positively correlated with the mean number of substitutions, while the number of transitions (p = 0.059) and transversions (p = 0.053) approached significance. There was no association between genetic diversity measures (nucleotide diversity, pairwise differences, or haplotype number) and the total number of tropical cyclones or major hurricanes.

4. Discussion

Our research reveals significant genetic structure and biogeographic patterns in Coccoloba uvifera, reflecting divergence during the Pleistocene epoch based on Bayesian and haplotype network analyses. We have identified three clades with the oldest divergence (1.78 mybp) of the Aruba–Trinidad–Tobago–Antigua–Jamaica Island group from the continental Belize–Florida–US Virgin Islands group, followed by a more recent 1.08 mybp divergence between the Belize and Florida–USVI groups. The network analysis supports these divergences with corresponding 14 and 11 predicted mutational events. Bayesian analysis identified a divergence (0.217 mybp) between the Aruba, Trinidad, and Tobago clade and the Antigua–Jamaica clade, although the network analysis does not support this. Considering the geology and proximity of these islands, it is plausible that the Antilles islands of Antigua and Jamaica diverged 0.217 mybp from the three islands (Aruba, Trinidad, and Tobago) located in close proximity to South America [45,46,47]. We observed a demographic expansion (0.324 mybp) of C. uvifera starting approximately 100,000 years before the Antilles (Antigua–Jamaica) divergence from the South American-adjacent sites (Aruba–Trinidad–Tobago) and peaking at roughly the last glacial maximum (ca. 0.026–0.019 mybp) when the global sea level low-stand was approximately 125 m lower [48].
The results of this intraspecific chloroplast molecular phylogeography suggest that current Coccoloba uvifera populations likely originated in South America and migrated north through Central America. This is an interesting finding because fossil leaves place the genus Coccoloba in Alaska and southeastern North America during the Paleocene (66–56 mybp) and Eocene (56–33.9 mybp), while fossil pollen from the Miocene (23–5.3 mybp) has been documented from coastal Mexico [6,8,9,10]. In the only molecular phylogeny of the genus Coccoloba, Koenemann and Burke [11] identified Mesoamerica as the likely origin for the genus, which is consistent with fossil records and the origin of the genus Coccoloba as North American. In his extensive studies of Coccoloba across the neotropics, Howard [2,12,49] noted C. uvifera as a significant component of the coastal strand vegetation and that it was widely distributed, with species found in Trinidad being essentially South American with dispersal northward [49]. Our results fit this general pattern; however, more extensive sampling across the native range, especially coastal South America (Columbia, Venezuela, and Suriname), Caribbean coastal Central America, and the Gulf of Mexico, is needed to better resolve C. uvifera dispersal northward.
Coccoloba uvifera naturally occurs in the coastal strand vegetation, which can be significantly impacted by wind, salt spray, and the storm surge of tropical cyclone storm events [2]. Genetic diversity was not correlated with the number of tropical cyclones, ranging from tropical storms to Category 5 hurricanes and major hurricanes, Category 3-5, passing within 60 miles of the location between 1842 and 2021. We found a significant positive association between the latitude and number of tropical cyclones, with Trinidad (13), Tobago (26), and Aruba (16) having the fewest recorded storms compared to Florida (81), Antigua (68), and St. John (67). A positive association was also found between latitude and the mean number of substitutions for our non-coding chloroplast gene regions. The positive association with latitude, the number of storms, and the mean number of substitutions implies broad spatial patterns. Coastal strand vegetation is naturally a disturbance-mediated community; therefore, C. uvifera may be less impacted by tropical storm events than tree species not found in the coastal strand vegetation ecotone. This same pattern of foundational species in dynamic systems, showing little change in genetic diversity following significant disturbances, is also seen in the dioecious aquatic plant Vallisneria americana Michx. [50] and in the giant kelp Macrocystis pyrifera (L.) C. Agardh [51].

5. Conclusions

This is the first intraspecific phytogeography study of the dioecious tropical tree species C. uvifera across the Caribbean Basin and Florida, using maternally inherited non-coding chloroplast regions. The results of this study support three broad clades roughly corresponding to a South American-associated island group (oldest), a Central America-associated group, and a North America-associated group (most recent). There was no association between genetic diversity and the number of tropical cyclones. However, we observed associations between latitude, the total number of tropical cyclones (TS-Cat. 5), and the average number of substitutions for our non-coding chloroplast genes. In addition, we acknowledge that including Caribbean coastal sites from South America, Central America, and the Gulf of Mexico could improve the spatial–temporal resolution of the Bayesian coalescence analyses.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d16090562/s1, Table S1: Coccoloba uvifera leaf collection location, year it was collected, unique individual code, haplotype assigned, GPS coordinates, and GenBank accession numbers. Table S2: The number of named tropical cyclones (tropical storm—Cat. 5) and major hurricanes (Cat. 3-5) passing within 60 nautical miles of the location. Data provided by NOAA (Historical Hurricane Tracks, https://coast.noaa.gov/hurricanes accessed 13 June 24).

Author Contributions

Conceptualization, D.J.G. and A.D.F.; methodology, all authors; analyses, D.J.G.; investigations, all authors; resources, all authors; data curation, all authors; writing—original draft preparation, D.J.G.; writing—review and editing, all authors; visualization, D.J.G. and B.K.S.; funding acquisition, D.J.G., L.A.D., D.P.W. and B.K.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by The Citadel Foundation (D.J.G.), The Citadel Undergraduate Research Experience (L.A.D., D.P.W., B.K.S.), and the Summer Undergraduate Research Experience (B.K.S.).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The new sequence data presented in this study are openly available in GenBank under the accession numbers PQ096171-PQ096425, respectively.

Acknowledgments

We thank two anonymous reviewers for suggestions on how to improve the manuscript. We thank Michael B. Thomas and the St. George Village Botanical Garden for providing the St. Croix, USVI, leaf material (DFW19050U) for DNA extractions. We thank landowners, St. George Village Botanical Garden, and The University of the West Indies Herbarium for permission to collect and their provision of leaf material for DNA extractions and scientific collection permits from the USDA National Parks Service for Canaveral National Seashore (CANA-2020-SCI-0002) and the Virgin Islands (VIIS-2020-SCI-0011). We also thank The Citadel, the Swain Family School of Science and Mathematics, and the Biology Department for their continued support of undergraduate research.

Conflicts of Interest

The authors declare no conflicts of interest. The funders had no role in the study’s design, the collection, analyses, or interpretation of data, the writing of the manuscript, or the decision to publish the results.

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Figure 1. Geographic distribution of 51 Coccoloba uvifera plants collected from nine locations across the Caribbean Basin and Florida. Twenty-six haplotypes were identified based on five concatenated non-coding chloroplast regions with a total length of approximately 4650 bps.
Figure 1. Geographic distribution of 51 Coccoloba uvifera plants collected from nine locations across the Caribbean Basin and Florida. Twenty-six haplotypes were identified based on five concatenated non-coding chloroplast regions with a total length of approximately 4650 bps.
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Figure 2. TCS haplotype maximum parsimony network analysis of 26 haplotypes based on the sequence of chloroplast non-coding regions from 51 Coccoloba uvifera plants sampled across the Caribbean Basin. The size of the circle reflects the number of individuals that share this haplotype. Color represents the source population, white nodes represent hypothesized unsampled haplotypes, and hash marks indicate the number of mutational differences.
Figure 2. TCS haplotype maximum parsimony network analysis of 26 haplotypes based on the sequence of chloroplast non-coding regions from 51 Coccoloba uvifera plants sampled across the Caribbean Basin. The size of the circle reflects the number of individuals that share this haplotype. Color represents the source population, white nodes represent hypothesized unsampled haplotypes, and hash marks indicate the number of mutational differences.
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Figure 3. Spherical phylogeography coalescent analysis of Coccoloba uvifera, using bModelTest evolutionary model averaging, indicated divergence between the Central American (Belize), North America (Florida), and U.S. Virgin Islands (USVI) group from the Aruba, Antigua, Trinidad, Tobago, and Jamaica island group approximately 1.78 mybp. The Belize group diverged from the Florida–USVI group around 1.08 mybp. The Antigua–Jamaica island group diverged from the Trinidad, Tobago, and Aruba island group by around 0.217 mybp. Bars indicate the 95% HPD intervals for the divergence times. The red arrow indicates the last glacial maximum (LGM).
Figure 3. Spherical phylogeography coalescent analysis of Coccoloba uvifera, using bModelTest evolutionary model averaging, indicated divergence between the Central American (Belize), North America (Florida), and U.S. Virgin Islands (USVI) group from the Aruba, Antigua, Trinidad, Tobago, and Jamaica island group approximately 1.78 mybp. The Belize group diverged from the Florida–USVI group around 1.08 mybp. The Antigua–Jamaica island group diverged from the Trinidad, Tobago, and Aruba island group by around 0.217 mybp. Bars indicate the 95% HPD intervals for the divergence times. The red arrow indicates the last glacial maximum (LGM).
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Figure 4. Coalescent Bayesian Skyline analysis of 51 Coccoloba uvifera plants sampled across the Caribbean Basin, based on five non-coding chloroplast regions. Effective population size increases from 1 million individuals (0.324 mybp) to 20.2 million individuals (0.028 mybp). Solid line represents the mean effective population size and dashed lines represent the 95% highest posterior density (HPD). The time scale is thousands of years before present (Kybp).
Figure 4. Coalescent Bayesian Skyline analysis of 51 Coccoloba uvifera plants sampled across the Caribbean Basin, based on five non-coding chloroplast regions. Effective population size increases from 1 million individuals (0.324 mybp) to 20.2 million individuals (0.028 mybp). Solid line represents the mean effective population size and dashed lines represent the 95% highest posterior density (HPD). The time scale is thousands of years before present (Kybp).
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Table 1. Coccoloba uvifera primers were designed for five non-coding chloroplast regions. The small single-copy region contained rpl32-trnL and ndhA intron while the large single-copy region contained rps16-trnK, psbD-trnT, and psbE-petL.
Table 1. Coccoloba uvifera primers were designed for five non-coding chloroplast regions. The small single-copy region contained rpl32-trnL and ndhA intron while the large single-copy region contained rps16-trnK, psbD-trnT, and psbE-petL.
RegionPrimer Sequence
rpl32-trnL5’-TCT CTT TCT ACC GGC AAT TCA-3’
5’-TCA TAA TTT CAA CAA ACC GAT TAA A-3’
ndhA intron5’-TCG TTG AGG CAT AAA TTT TCC AA-3’
5’-ACC TCA TAC GGC TCC TCG AG-3’
rps16-trnK5’-TGT ATC ACA GCA AAT TCA ACG AA-3’
5’-TTC TTG AAA GGG GCG CTC AA-3’
psbD-trnT5’-TCC GAT AAG GGG CTT TTT ACT-3’
5’-GCA CCT GAC CCA TGA ATT GT-3’
psbE-petL5’-TCA GAC ATG CTC AGC TCC AC-3’
5’-TTT TGT GAA AGA TAG GAG CGA AA-3’
Table 2. Molecular diversity of Coccoloba uvifera based on chloroplast haplotypes generated from 5 to 7 individuals per location and five concatenated non-coding chloroplast regions (rpl32-trnL, ndhA intron, rps16-trnK, psbD-trnT, and psbE-petL).
Table 2. Molecular diversity of Coccoloba uvifera based on chloroplast haplotypes generated from 5 to 7 individuals per location and five concatenated non-coding chloroplast regions (rpl32-trnL, ndhA intron, rps16-trnK, psbD-trnT, and psbE-petL).
Statistics.AntiguaArubaBelizeFloridaJamaicaTrinidadTobagoSt.JohnSt.Croix
Sample size755556576
No. haplotypes333525376
No. of transitions16013231510
No. of transversions0133191200817
No. of substitutions11933214311327
No. of indels162782158
No. of polymorphic sites22553922521835
No. private subst. sites000410043
Mean No. Pairwise Differences 0.5715216.68.81.90.86.717.1
pairwise differences (SD)0.528.11.38.94.91.20.73.68.9
Nucleotide Diversity (p)0.0001220.0032070.0042800.0035490.0018820.0003990.0001710.0014250.003663
Nucleotide Diversity (SD)0.0001280.0020280.0033600.0022350.0012250.0003050.0001700.0008770.002200
Table 3. Analysis of molecular variance (AMOVA) of nine populations of Coccoloba uvifera sampled across the Caribbean Basin. Significant genetic structure was identified, with approximately 54% of the haplotype variation due to differences among populations and 46% within populations (ϕST = 0.5393, p < 0.0001).
Table 3. Analysis of molecular variance (AMOVA) of nine populations of Coccoloba uvifera sampled across the Caribbean Basin. Significant genetic structure was identified, with approximately 54% of the haplotype variation due to differences among populations and 46% within populations (ϕST = 0.5393, p < 0.0001).
Source of Sum ofVariance Percentage
Variationd.f.SquaresComponentsof Variation
Among
Populations8225.764.34 Va53.93
Within
Populations42155.613.71 Vb46.07
Total50381.378.04
Table 4. Correlation analysis assessing diversity measures by site latitude, the total number of tropical cyclones (TS-Cat. 5), and the total number of major hurricanes (Cat.3-5) passing within 60 miles of the location between 1842 and 2021 (Historical Hurricane Tracks provided by https://coast.noaa.gov/hurricanes (accessed on 12 June 2024)). Correlation coefficient, p value, and number of samples.
Table 4. Correlation analysis assessing diversity measures by site latitude, the total number of tropical cyclones (TS-Cat. 5), and the total number of major hurricanes (Cat.3-5) passing within 60 miles of the location between 1842 and 2021 (Historical Hurricane Tracks provided by https://coast.noaa.gov/hurricanes (accessed on 12 June 2024)). Correlation coefficient, p value, and number of samples.
LatitudePairwiseNucleotide HaplotypesTransitionsTransversionsSubstitutionsTS-Cat. 5Cat. 3-5
DifferencesDiversity (TS)(TV)(Sub)
Latitude-0.5200.5200.2510.6480.6600.6790.8620.400
0.1520.1520.5150.0590.0530.0440.0030.287
99999999
Pairwise Differences -1.0000.3040.8810.9720.9720.2420.095
<0.0010.4260.002<0.001<0.0010.530.809
9999999
Nucleotide Diversity -0.3080.8820.9720.9720.2420.096
0.4200.001<0.001<0.0010.5310.807
999999
Haplotypes -0.5720.2830.4030.3510.430
0.1070.4610.2830.3540.248
99999
Transitions (TS) -0.8560.9410.4160.127
0.003<0.0010.2660.744
9999
Transversions (TV) -0.9800.3810.187
<0.0010.3130.629
990.9
Substitution (Sub) -0.4070.171
0.2770.66
99
TS-Cat. 5 -0.745
0.021
9
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MDPI and ACS Style

Gustafson, D.J.; Dix, L.A.; Webster, D.P.; Scott, B.K.; Gustafson, I.E.; Farrell, A.D.; Koenemann, D.M. Phylogeography of Coccoloba uvifera (Polygonaceae) Sampled across the Caribbean Basin. Diversity 2024, 16, 562. https://doi.org/10.3390/d16090562

AMA Style

Gustafson DJ, Dix LA, Webster DP, Scott BK, Gustafson IE, Farrell AD, Koenemann DM. Phylogeography of Coccoloba uvifera (Polygonaceae) Sampled across the Caribbean Basin. Diversity. 2024; 16(9):562. https://doi.org/10.3390/d16090562

Chicago/Turabian Style

Gustafson, Danny J., Logan A. Dix, Derek P. Webster, Benjamin K. Scott, Isabella E. Gustafson, Aidan D. Farrell, and Daniel M. Koenemann. 2024. "Phylogeography of Coccoloba uvifera (Polygonaceae) Sampled across the Caribbean Basin" Diversity 16, no. 9: 562. https://doi.org/10.3390/d16090562

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