High genetic structure and low mitochondrial diversity in bottlenose dolphins of the Archipelago of Bocas del Toro, Panama: A population at risk?

<div><p>The current conservation status of the bottlenose dolphin (<i>Tursiops truncatus</i>) under the IUCN is ‘least concern’. However, in the Caribbean, small and localized populations of the ‘inshore form’ may be at higher risk of extinction than the ‘worldwide distributed form’ due to a combination of factors including small population size, high site fidelity, genetic isolation, and range overlap with human activities. Here, we study the population genetic structure of bottlenose dolphins from the Archipelago of Bocas del Toro in Panama. This is a small population characterized by high site fidelity and is currently heavily-impacted by the local dolphin-watching industry. We collected skin tissue samples from 25 dolphins to study the genetic diversity and structure of this population. We amplified a portion of the mitochondrial Control Region (mtDNA-CR) and nine microsatellite loci. The mtDNA-CR analyses revealed that dolphins in Bocas del Toro belong to the ‘inshore form’, grouped with the Bahamas-Colombia-Cuba-Mexico population unit. They also possess a unique haplotype new for the Caribbean. The microsatellite data indicated that the Bocas del Toro dolphin population is highly structured, likely due to restricted movement patterns. Previous abundance estimates obtained with mark-recapture methods reported a small population of 80 dolphins (95% CI = 72–87), which is similar to the contemporary effective population size estimated in this study (<i>Ne</i> = 73 individuals; CI = 18.0 - ∞; 0.05). The combination of small population size, high degree of genetic isolation, and intense daily interactions with dolphin-watching boats puts the Bocas del Toro dolphin to at high risk of extinction. Despite national guidelines to regulate the dolphin-watching industry in Bocas del Toro and ongoing educational programs for tour operators, only in 2012 seven animals have died due to boat collisions. Our results suggest that the conservation status of bottlenose dolphins in Bocas del Toro should be elevated to ‘endangered’ at the national level, as a precautionary measure while population and viability estimates are conducted.</p></div

Beta diversity indices of prokaryotes and eukaryotes by ulcer size.

Beta diversity of prokaryotes (A) and eukaryotes (B) based on the sample type (healthy skin (Healthy) or the lesion (Lesion)) divided by ulcer size (categorized into quartiles: Q1 = 150mm, Q2 = 151-245mm, Q3 = 246-501mm, Q4 = 502-1963mm). There are not significant differences between ulcer size groups. (TIF)</p

Geographical sampling locations.

Map illustrating the geographical locations from which samples were collected in Colombia. Includes an explanation of the sample codification system, which is based on the initials of the collection sites (B = Bonza, G = Guaviare, M = Medellín), the sample type (L = Skin Lesion, S = Healthy Skin) and a unique numerical identifier (e.g., BL-13). The map was constructed using QGIS version 2.18.7. Basemap: Elevation/World_Hillshade https://bit.ly/3vVQ1lL; Sources: Esri, Airbus DS, USGS, NGA, NASA, CGIAR, N Robinson, NCEAS, NLS, OS, NMA, Geodatastyrelsen, Rijkswaterstaat, GSA, Geoland, FEMA. (TIF)</p

Genetic diversity values for nine microsatellites loci in six <i>Tursiops truncatus</i> populations units analyzed (Panama, Costa Rica, The Bahamas, Colombia-Honduras-PuertoRico, Cuba, and Mexico).

<p>For each location, we include sample size (<i>n</i>). For each locus we include: total number of alleles (<i>N</i>_<i>A</i>), allelic richness (<i>AR</i>), observed (<i>H</i>_<i>O</i>), and expected (<i>H</i>_<i>E</i>) heterozygosity. Loci out of <i>HWE</i> after Bonferroni correction (0.001562) are in bold.</p

<i>D-loop</i> haplotype frequency distribution among Caribbean bottlenose dolphin populations according to Caballero and Islas-Villanueva et al. [3].

<p>New haplotypes reported in this study (<i>TruBOC</i> from Bocas del Toro, and <i>TtruCR1</i> and <i>TruCR2</i> from Costa Rica) are in bold.</p

Beta diversity indices of prokaryotes and eukaryotes by <i>Leishmania</i> species.

Beta diversity of prokaryotes (A) and eukaryotes (B) based on the sample type (healthy skin (Healthy) or the lesion (Lesion)) divided by Leishmania species. There are not significant differences between species groups. (TIF)</p

Alpha diversity indices of prokaryotes and eukaryotes by <i>Leishmania</i> species.

Alpha diversity indices of prokaryotes (A) and eukaryotes (B) based on the sample type (healthy skin (Healthy) or the lesion (Lesion)) divided by Leishmania species (L.b = L. braziliensis, L.b/Ln. = L. braziliensis/L. naiffi, L.b/Ln./L.p-g = L. braziliensis/L. naiffi/L.panamensis-guyanenensis complex, L.p-g = L.panamensis-guyanenensis). There are not significant differences between species groups. (TIF)</p

Relative abundance of <i>Leishmania</i> species.

The abundance is expressed in percentage (%) related with the analyzed samples found in CL patients from three geographical locations in Colombia (Bonza, Guaviare, Medellín), focusing on those with an abundance greater than 5%.</p

Correlation analysis between prokaryotic genus and parasitic load.

Correlation analysis showing the abundance values of the genus Acinetobacter, the only significant genus in this analysis. Spearman’s correlation test was applied, and the resulting coefficient (R) and p-value are clearly indicated.</p

Population differentiation of <i>Tursiops truncatus</i> between pairwise populations in the Caribbean obtained with mtDNA-CR.

<p>High and significant values are indicated in bold and the <i>P-value</i> is shown below each value (<i>P-values</i> were obtained after 1000 permutations). <i>Ф</i>_<i>ST</i> values are indicated below the diagonal. <i>F</i>_<i>ST</i> values are above diagonal.</p