Genetic diversity
Our results indicate that integrating both asexual and sexual to |restore the Cuevones Reef has proven successful in retaining levels of genetic diversity comparable to those found in natural reefs. This is highly significant for restoration programs as it enables the preservation of genetic diversity and increases resilience, consequently, improving conservation efforts of coral reefs in the region in the face of local disturbances and global threats. Particularly, after the massive bleaching event caused by the Niño 2023 event16,20,32.
Previous studies have documented that utilizing local populations in restoration efforts maintains a pre-existing genetic identity and reinstates historical patterns of genetic diversity7. Furthermore, introducing diverse genotypes from various locations in the Mexican Caribbean reef is expected to expedite its recovery and enhance its resilience. Introducing genotypes from different locations can help maintain or even improve the genetic variability of coral populations. According to DeFilippo et al. (2022), with sufficient natural genetic variation, corals are more likely to adapt to warming temperatures and other stressors. Therefore, restoration programs should prioritize maintaining and enhancing the genetic variation of populations, which may be more effective in the long term than strategies based solely on introducing heat-tolerant genotypes.
Although the diversity of the Cuevones reef is comparatively high within the scope of this study, our observed heterozygosity (He) values for A. palmata (He = 0.125–0.167) are relatively lower than those reported in other regional studies in the eastern and western Caribbean and the Mexican Caribbean. Specifically, studies using SNP markers in the region reported He values ranging from 0.195 to 0.21622. In microsatellite studies, Gómez-Campo (2015) reported He values between 0.763 and 0.812 for A. palmata at seven locations in the Mexican Caribbean; Baums et al. (2008) reported an average He of 0.76 for the Caribbean region. Meanwhile, Domínguez-Maldonado et al. (2022) reported an average He of 0.315 for the Mexican Caribbean and the Gulf of Mexico. Hence, our findings on diversity in natural populations may reflect the ongoing population bottlenecks this species faces within the Caribbean region. These populations persist under continued threat, experiencing significant and repeated mortality events. Thus, there is an urgent need to standardize restoration techniques to ensure the recovery efforts for these populations23,50.
Recognized as one of the Mesoamerican Reef System's best-preserved reefs, Limones Reef displays notable diversity values (H = 3.25 and He = 0.14). This could be attributed to the protective measures implemented by government and academic institutions, including the Autonomous University of Mexico (UNAM), the National Fisheries Institute (INAPESCA), and the National Commission for Protected Natural Areas (CONANP). For instance, shortly after hurricanes Emily and Wilma in 2005, the Puerto Morelos Reef National Park (PMRNP) initiated rehabilitation efforts, relocating 221 coral fragments between the reef lagoon and the Limones reef crest66. This intervention likely contributed to the preservation of coral cover at the site. Unfortunately, there was no subsequent monitoring of this initiative, so how many fragments initially survived and how many are still alive to date, is unknown.
In mid-2012, the A. palmata coverage on this reef exceeded 30%, closely resembling the reported figures for reefs in the northeastern Yucatan Peninsula during the late 1970s40,41. In 2019, Drury et al. found a positive correlation between genetic diversity and coral cover, hinting at potential associations with complementarity, influencing cover through niche partitioning, and/or interactions among genets. The high genetic diversity observed at Limones Reef may be attributed to local oceanographic conditions conducive to forming eddies52, potentially facilitating larval retention and accumulation73. These conditions likely contributed to the natural recovery of A. palmata at the site, as indicated by Rodríguez-Martínez et al. (2014), who documented a high proportion of small colonies and minimal partial mortality of this species. This is the first genetic study carried out on this reef, and the results will allow us to better inform the necessary actions to preserve the condition of the Limones Reef.
Also, our study's observed diversity among individuals is noteworthy; among the 128 A. palmata colonies analyzed, only 7% were identified as clonal. Previous genetic analyses of A. palmata have shown that reefs can often be monoclonal or consist of a limited number of genotypes (genets) 6,11. In addition, in high-throughput sequencing studies with high marker density, each sample is usually composed of a single genotype74. Gómez-Campo (2015) identified 130 (44%) genotypes from 297 samples over an area of 324 km in a microsatellite study conducted in Quintana Roo (Cancún-Xcalak). The sampling, including the collection of clones was carried out using the polar plot method.
Genetic Structure
We identified subtle genetic differentiation among populations of A. palmata (FST = 0.012, p = 0.02) in northern Quintana Roo. We found genetic differentiation between the Cadenita and Akumal reefs, which are approximately 143 km apart. This result is consistent with the findings of Drury et al. (2017), where utilizing SNPs from a reduced-representation sequencing approach in the threatened coral A. cervicornis revealed the population structure within the Florida Reef Tract, even at the level of individual reefs, likely attributed to the presence of unique alleles. However, Cadenita and Farito, separated by only about 1.68 km showed the greatest genetic differentiation (FST = 0.076). In Farito, only three colonies of A. palmata were found during sampling. This is probably due to the population decline and consequent loss of genetic variability at this touristic site.
Previous genetic studies on Acroporids have shown variable results, suggesting the influence of spatial scale on patterns of genetic structure. Nonetheless, it is worth mentioning that SNP markers detect subtle genetic differences at local scales in populations where other markers, such as microsatellites had not identified them. For example, Gómez-Campo (2015) found no genetic structure in A. palmata populations in the Mexican Caribbean, suggesting that it is a panmictic population (FST = 0.000, p = 0.474). In contrast, other studies have found a significant regional structure for populations separated by more than 500 km in nuclear and mitochondrial genes3,51. In the Florida Reef Tract, analysis of A. cervicornis using microsatellites showed little population differentiation and no significant population structure10. These results were confirmed with mitochondrial control region sequences that showed no significant population structure for A. cervicornis at the same site (Hemond & Vollmer, 2010). However, significant genetic differentiation was evident when the analysis was extended to broader scales at the Caribbean level10. Drury et al. (2016) showed population structure in the Florida Reef Tract and high diversity within A. cervicornis populations for the first time through SNP markers scored by Genotyping by Sequencing (GBS).
The results of the AMOVA in this study reveal that the predominant variation exists within populations (98.86%). This variation can be attributed to the subtle genetic structure within the population, where individuals from different subpopulations (reefs) show minimal genetic distance. This suggests ongoing sexual reproduction and a potential lack of barriers between the studied reefs45. High intra-population genetic variation may confer resilience to stressors and climate change factors, including temperature anomalies and acidification25. In the scenario where populations are interconnected, restoring a deteriorated reef becomes achievable solely through recruiting larvae from distant and well-preserved reefs, exemplified by the Limones and Bajito Nizuc reefs. Therefore, these two reefs could be functioning as source reefs, playing a crucial role in sustaining the A. palmata populations in the northern Mexican Caribbean. This genetic exchange could accelerate the adaptation process by introducing favorable alleles from one population to another, although there is also the probability of contributing non-adaptive alleles1. This information is essential for formulating effective policies and managing resources efficiently. Understanding genetic connectivity provides essential insights into how populations are maintained and replenished after environmental disturbances. It also serves as a valuable indicator of population resilience75.
Environmental factors such as ocean currents and the life cycle of Acropora species must also be taken into consideration in explaining their genetic connectivity. There is a notable correlation between ocean surface currents and larval dispersal routes, suggesting that species with planktonic larvae inhabiting regions connected by currents tend to show high genetic similarity65. In the case of A. palmata, after fertilization, larvae undergo a developmental period of 78 hours before displaying the first signs of motility6. Pelagic larvae become competent to settle within 5 days but can remain planktonic for up to 20 days5, supplying a chance for dispersal and gene flow between reefs. This extended planktonic phase not only allows for the colonization of distant reefs but also eases gene flow between populations, contributing to the observed connectivity and genetic exchange between reefs in the northern Quintana Roo region.
DNA sequencing studies reveal a considerable amount of diversity yet to be described, and their evolutionary and ecological implications35,12. Our understanding of the potential impacts of genotypic diversity or genet-genet interactions on community function in marine ecosystems is yet limited72. Therefore, further exploration of persisting coral populations at the genomic level is imperative to unravel the intricate relationships between genetic diversity and the ecological dynamics of coral reef ecosystems.