Saenz-Agudelo Pablo

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  • Preprint
    Marine dispersal scales are congruent over evolutionary and ecological time
    ( 2016-10) Pinsky, Malin L. ; Saenz-Agudelo, Pablo ; Salles, Océane C. ; Almany, Glenn R. ; Bode, Michael ; Berumen, Michael L. ; Andrefouet, Serge ; Thorrold, Simon R. ; Jones, Geoffrey P. ; Planes, Serge
    The degree to which offspring remain near their parents or disperse widely is critical for understanding population dynamics, evolution, and biogeography, and for designing conservation actions. In the ocean, most estimates suggesting short-distance dispersal are based on direct ecological observations of dispersing individuals, while indirect evolutionary estimates often suggest substantially greater homogeneity among populations. Reconciling these two approaches and their seemingly competing perspectives on dispersal has been a major challenge. However, here we show for the first time that evolutionary and ecological measures of larval dispersal can closely agree by using both to estimate the distribution of dispersal distances. In orange clownfish (Amphiprion percula) populations in Kimbe Bay, Papua New Guinea, we found that evolutionary dispersal kernels were 17 [95% CI: 12–24] km wide, while an exhaustive set of direct larval dispersal observations suggested kernel widths of 27 [19–36] km or 19 [15–27] km across two years. The similarity between these two approaches suggests that ecological and evolutionary dispersal kernels can be equivalent, and that the apparent disagreement between direct and indirect measurements can be overcome. Our results suggest that carefully applied evolutionary methods, which are often less expensive, can be broadly relevant for understanding ecological dispersal across the tree of life.
  • Preprint
    Connectivity dominates larval replenishment in a coastal reef fish metapopulation
    ( 2011-01-25) Saenz-Agudelo, Pablo ; Jones, Geoffrey P. ; Thorrold, Simon R. ; Planes, Serge
    Direct estimates of larval retention and connectivity are essential to understand the structure and dynamics of marine metapopulations, and optimize the size and spacing of reserves within networks of marine protected areas (MPAs). For coral reef fishes, while there are some empirical estimates of self-recruitment at isolated populations, exchange among sub-populations has been rarely quantified. Here we used microsatellite DNA markers and a likelihood-based parentage analysis to assess the relative magnitude of self-recruitment and exchange among 8 geographically distinct sub-populations of the panda clownfish Amphiprion polymnus along 30 km of coastline near Port Moresby, Papua New Guinea. In addition, we used an assignment/exclusion test to identify immigrants arriving from genetically distinct sources. Overall, 82% of the juveniles were immigrants while 18% were progeny of parents genotyped in our focal metapopulation. Of the immigrants, only 6% were likely to be genetically distinct from the focal metapopulation, suggesting most of the connectivity is among sub-populations from a rather homogeneous genetic pool. Of the 18% that were progeny of known adults, two thirds dispersed among the 8 sub-populations and only one third settled back into natal sub- populations. Comparison of our data with previous studies suggested that variation in dispersal distances is likely to be influenced by the geographic setting and spacing of sub-populations.
  • Article
    Novel polymorphic microsatellite markers developed for a common reef sponge, Stylissa carteri
    (Springer, 2013-04-04) Giles, Emily C. ; Saenz-Agudelo, Pablo ; Berumen, Michael L. ; Ravasi, Timothy
    Despite the ubiquitous role sponges play in reef ecosystem dynamics, little is known about population-level connectivity in these organisms. The general field of population genetics in sponges remains in its infancy. To date, microsatellite markers have only been developed for few sponge species and no sponge population genetics studies using microsatellites have been conducted in the Red Sea. Here, with the use of next-generation sequencing, we characterize 12 novel polymorphic loci for the common reef sponge, Stylissa carteri. The number of alleles per loci ranged between three and eight. Observed heterozygosity frequencies (Ho) ranged from 0.125 to 0.870, whereas expected (He) heterozygosity frequencies ranged from 0.119 to 0.812. Only one locus showed consistent deviations from Hardy-Weinberg equilibrium (HWE) in both populations and two loci consistently showed the possible presence of null alleles. No significant linkage disequilibrium was detected for any pairs of loci. These microsatellites will be of use for numerous ecological studies focused on this common and abundant sponge.
  • Article
    Seascape and life-history traits do not predict self-recruitment in a coral reef fish
    (The Royal Society, 2016-08-09) Herrera, Marcela ; Nanninga, Gerrit ; Planes, Serge ; Jones, Geoffrey P. ; Thorrold, Simon R. ; Saenz-Agudelo, Pablo ; Almany, Glenn R. ; Berumen, Michael L.
    The persistence and resilience of many coral reef species are dependent on rates of connectivity among sub-populations. However, despite increasing research efforts, the spatial scale of larval dispersal remains unpredictable for most marine metapopulations. Here, we assess patterns of larval dispersal in the angelfish Centropyge bicolor in Kimbe Bay, Papua New Guinea, using parentage and sibling reconstruction analyses based on 23 microsatellite DNA loci. We found that, contrary to previous findings in this system, self-recruitment (SR) was virtually absent at both the reef (0.4–0.5% at 0.15 km2) and the lagoon scale (0.6–0.8% at approx. 700 km2). While approximately 25% of the collected juveniles were identified as potential siblings, the majority of sibling pairs were sampled from separate reefs. Integrating our findings with earlier research from the same system suggests that geographical setting and life-history traits alone are not suitable predictors of SR and that high levels of localized recruitment are not universal in coral reef fishes.
  • Article
    Rank change and growth within social hierarchies of the orange clownfish, Amphiprion percula
    (Springer, 2022-10-05) Fitzgerald, Lucy M. ; Harrison, Hugo B. ; Coker, Darren J. ; Sáenz-Agudelo, Pablo ; Srinivasan, Maya ; Majoris, John E. ; Boström Einarsson, Lisa ; Pujol, Benoit ; Bennett-Smith, Morgan ; Thorrold, Simon R. ; Planes, Serge ; Jones, Geoffrey P. ; Berumen, Michale L.
    Social hierarchies within groups define the distribution of resources and provide benefits that support the collective group or favor dominant members. The progression of individuals through social hierarchies is a valuable characteristic for quantifying population dynamics. On coral reefs, some clownfish maintain size-based hierarchical communities where individuals queue through social ranks. The cost of waiting in a lower-ranked position is outweighed by the reduced risk of eviction and mortality. The orange clownfish,Amphiprion percula, maintains stable social groups with subordinate individuals queuing to be part of the dominant breeding pair. Strong association with their host anemone, complex social interactions, and relatively low predation rates make them ideal model organisms to assess changes in group dynamics through time in their natural environment. Here, we investigate the rank changes and isometric growth rates ofA. percula from 247 naturally occurring social groups in Kimbe Island, Papua New Guinea (5° 12′ 13.54″ S, 150° 22′ 32.69″ E). We used DNA profiling to assign and track individuals over eight years between 2011 and 2019. Over half of the individuals survived alongside two or three members of their original social group, with twelve breeding pairs persisting over the study period. Half of the surviving individuals increased in rank and experienced double the growth rate of those that maintained their rank. Examining rank change in a wild fish population provides new insights into the complex social hierarchies of reef fishes and their role in social evolution.
  • Article
    Characterization of new microsatellite loci for population genetic studies in the Smooth Cauliflower Coral (Stylophora sp.)
    (Springer, 2013-01-09) Banguera-Hinestroza, Eulalia ; Saenz-Agudelo, Pablo ; Bayer, Till ; Berumen, Michael L. ; Voolstra, Christian R.
    A total of one hundred microsatellites loci were selected from the draft genome of Stylophora pistillata and evaluated in previously characterized samples of Stylophora cf pistillata from the Red Sea. 17 loci were amplified successfully and tested in 24 individuals from samples belonging to a single population from the central region of the Red Sea. The number of alleles ranged from 3 to 15 alleles per locus, while observed heterozygosity ranged from 0.292 to 0.95. Six of these loci showed significant deviations from Hardy–Weinberg equilibrium (HWE) expectations, and 4/136 paired loci comparisons suggested linkage disequilibrium after Bonferroni corrections. After excluding loci with significant HWE deviation and evidence of null alleles, average genetic diversity over loci in the population studied (N = 24, Nloci = 11) was 0.701 ± 0.380. This indicates that these loci can be used effectively to evaluate genetic diversity and undertake population genetics studies in Stylophora sp. populations.
  • Preprint
    First genealogy for a wild marine fish population reveals multi-generational philopatry
    ( 2016-10) Salles, Océane C. ; Pujol, Benoit ; Maynard, Jeffrey A. ; Almany, Glenn R. ; Berumen, Michael L. ; Jones, Geoffrey P. ; Saenz-Agudelo, Pablo ; Srinivasan, Maya ; Thorrold, Simon R. ; Planes, Serge
    Natal philopatry — the return of individuals to their natal area for reproduction — has advantages and disadvantages for animal populations. Natal philopatry may generate local genetic adaptation but may also increase the probability of inbreeding that can compromise persistence. While natal philopatry is well documented in anadromous fishes, marine fish may also return to their birth site to spawn. How philopatry shapes wild fish populations is, however, unclear because it requires constructing multi-generational pedigrees that are currently lacking for marine fishes. Here we present the first multi-generational pedigree for a marine fish population by repeatedly genotyping all individuals in a population of the orange clownfish (Amphiprion percula) at Kimbe Island (Papua New Guinea) over a 10-year period. Based on 2927 individuals, our pedigree analysis revealed that longitudinal philopatry was recurrent over five generations. Progeny tended to settle close to their parents, with related individuals often sharing the same colony. However, successful inbreeding was rare and genetic diversity remained high, suggesting occasional inbreeding does not impair local population persistence. Local reproductive success was dependent on the habitat larvae settled into, rather than the habitat they came from. Our study suggests that longitudinal philopatry can influence both population replenishment and local adaptation of marine fishes. Resolving multi-generational pedigrees over a relatively short time period, as we present here, provides a framework for assessing the ability of marine populations to persist and adapt to accelerating climate change.
  • Article
    Pieces in a global puzzle: population genetics at two whale shark aggregations in the western Indian Ocean
    (Wiley Open Access, 2022-01-25) Hardenstine, Royale S. ; He, Song ; Cochran, Jesse E. M. ; Braun, Camrin D. ; Cagua, E. Fernando ; Pierce, Simon J. ; Prebble, Clare E. M. ; Rohner, Christoph A. ; Saenz-Agudelo, Pablo ; Sinclair-Taylor, Tane H. ; Skomal, Gregory B. ; Thorrold, Simon R. ; Watts, Alexandra M. ; Zakroff, Casey ; Berumen, Michael L.
    The whale shark Rhincodon typus is found throughout the world's tropical and warm-temperate ocean basins. Despite their broad physical distribution, research on the species has been concentrated at a few aggregation sites. Comparing DNA sequences from sharks at different sites can provide a demographically neutral understanding of the whale shark's global ecology. Here, we created genetic profiles for 84 whale sharks from the Saudi Arabian Red Sea and 72 individuals from the coast of Tanzania using a combination of microsatellite and mitochondrial sequences. These two sites, separated by approximately 4500 km (shortest over-water distance), exhibit markedly different population demographics and behavioral ecologies. Eleven microsatellite DNA markers revealed that the two aggregation sites have similar levels of allelic richness and appear to be derived from the same source population. We sequenced the mitochondrial control region to produce multiple global haplotype networks (based on different alignment methodologies) that were broadly similar to each other in terms of population structure but suggested different demographic histories. Data from both microsatellite and mitochondrial markers demonstrated the stability of genetic diversity within the Saudi Arabian aggregation site throughout the sampling period. These results contrast previously measured declines in diversity at Ningaloo Reef, Western Australia. Mapping the geographic distribution of whale shark lineages provides insight into the species’ connectivity and can be used to direct management efforts at both local and global scales. Similarly, understanding historical fluctuations in whale shark abundance provides a baseline by which to assess current trends. Continued development of new sequencing methods and the incorporation of genomic data could lead to considerable advances in the scientific understanding of whale shark population ecology and corresponding improvements to conservation policy.
  • Preprint
    Estimating connectivity in marine populations : an empirical evaluation of assignment tests and parentage analysis under different gene flow scenarios
    ( 2008-11-21) Saenz-Agudelo, Pablo ; Jones, Geoffrey P. ; Thorrold, Simon R. ; Planes, Serge
    The application of spatially explicit models of population dynamics to fisheries management and the design marine reserves network systems has been limited due to a lack of empirical estimates of larval dispersal. Here we compared assignment tests and parentage analysis for examining larval retention and connectivity under two different gene flow scenarios using panda clownfish (Amphiprion polymnus) in Papua New Guinea. A metapopulation of panda clownfish in Bootless Bay with little or no genetic differentiation among 5 spatially discrete locations separated by 2-6km provided the high gene flow scenario. The low gene flow scenario compared the Bootless Bay metapopulation with a genetically distinct population (Fst = 0.1) located at Schumann Island, New Britain, 1,500km to the north-east. We used assignment tests and parentage analysis based on microsatellite DNA data to identify natal origins of 177 juveniles in Bootless Bay and 73 juveniles at Schumann Island. At low rates of gene flow, assignment tests correctly classified juveniles to their source population. On the other hand, parentage analysis led to an overestimate of self-recruitment within the two populations due to the significant deviation from panmixia when both populations were pooled. At high gene flow (within Bootless Bay), assignment tests underestimated self-recruitment and connectivity among subpopulations, and grossly overestimated self-recruitment within the overall metapopulation. However, the assignment tests did identify immigrants from distant (genetically distinct) populations. Parentage analysis clearly provided the most accurate estimates of connectivity in situations of high gene flow.
  • Preprint
    Coral reef fish populations can persist without immigration
    ( 2015-10) Salles, Océane C. ; Maynard, Jeffrey A. ; Joannides, Marc ; Barbu, Corentin M. ; Saenz-Agudelo, Pablo ; Almany, Glenn R. ; Berumen, Michael L. ; Thorrold, Simon R. ; Jones, Geoffrey P. ; Planes, Serge
    Determining the conditions under which populations may persist requires accurate estimates of demographic parameters, including immigration, local reproductive success, and mortality rates. In marine populations, empirical estimates of these parameters are rare, due at least in part to the pelagic dispersal stage common to most marine organisms. Here, we evaluate population persistence and turnover for a population of orange clownfish, Amphiprion percula, at Kimbe Island in Papua New Guinea. All fish in the population were sampled and genotyped on five occasions at 2-year intervals spanning eight years. The genetic data enabled estimates of reproductive success retained in the same population (reproductive success to self-recruitment), reproductive success exported to other subpopulations (reproductive success to local connectivity), and immigration and mortality rates of sub-adults and adults. Approximately 50% of the recruits were assigned to parents from the Kimbe Island population and this was stable through the sampling period. Stability in the proportion of local and immigrant settlers is likely due to: low annual mortality rates and stable egg production rates, and the short larval stages and sensory capacities of reef fish larvae. Biannual mortality rates ranged from 0.09 to 0.55 and varied significantly spatially. We used these data to parameterize a model that estimated the probability of the Kimbe Island population persisting in the absence of immigration. The Kimbe Island population was found to persist without significant immigration. Model results suggest the island population persists because the largest of the subpopulations are maintained due to having low mortality and high self-recruitment rates. Our results enable managers to appropriately target and scale actions to maximize persistence likelihood as disturbance frequencies increase.
  • Preprint
    On minimising assignment errors and the trade‐off between false positives and negatives in parentage analysis
    ( 2013-05) Harrison, Hugo B. ; Saenz-Agudelo, Pablo ; Planes, Serge ; Jones, Geoffrey P. ; Berumen, Michael L.
    Genetic parentage analyses provide a practical means with which to identify parent–offspring relationships in the wild. In Harrison et al.'s study (2013a), we compare three methods of parentage analysis and showed that the number and diversity of microsatellite loci were the most important factors defining the accuracy of assignments. Our simulations revealed that an exclusion-Bayes theorem method was more susceptible to false-positive and false-negative assignments than other methods tested. Here, we analyse and discuss the trade-off between type I and type II errors in parentage analyses. We show that controlling for false-positive assignments, without reporting type II errors, can be misleading. Our findings illustrate the need to estimate and report both the rate of false-positive and false-negative assignments in parentage analyses.
  • Article
    Taxonomic, spatial and temporal patterns of bleaching in anemones inhabited by anemonefishes
    (Public Library of Science, 2013-08-08) Hobbs, Jean-Paul A. ; Frisch, Ashley J. ; Ford, Benjamin M. ; Thums, Michele ; Saenz-Agudelo, Pablo ; Furby, Kathryn A. ; Berumen, Michael L.
    Rising sea temperatures are causing significant destruction to coral reef ecosystems due to coral mortality from thermally-induced bleaching (loss of symbiotic algae and/or their photosynthetic pigments). Although bleaching has been intensively studied in corals, little is known about the causes and consequences of bleaching in other tropical symbiotic organisms. This study used underwater visual surveys to investigate bleaching in the 10 species of anemones that host anemonefishes. Bleaching was confirmed in seven anemone species (with anecdotal reports of bleaching in the other three species) at 10 of 19 survey locations spanning the Indo-Pacific and Red Sea, indicating that anemone bleaching is taxonomically and geographically widespread. In total, bleaching was observed in 490 of the 13,896 surveyed anemones (3.5%); however, this percentage was much higher (19–100%) during five major bleaching events that were associated with periods of elevated water temperatures and coral bleaching. There was considerable spatial variation in anemone bleaching during most of these events, suggesting that certain sites and deeper waters might act as refuges. Susceptibility to bleaching varied between species, and in some species, bleaching caused reductions in size and abundance. Anemones are long-lived with low natural mortality, which makes them particularly vulnerable to predicted increases in severity and frequency of bleaching events. Population viability will be severely compromised if anemones and their symbionts cannot acclimate or adapt to rising sea temperatures. Anemone bleaching also has negative effects to other species, particularly those that have an obligate relationship with anemones. These effects include reductions in abundance and reproductive output of anemonefishes. Therefore, the future of these iconic and commercially valuable coral reef fishes is inextricably linked to the ability of host anemones to cope with rising sea temperatures associated with climate change.
  • Preprint
    The status of coral reef ecology research in the Red Sea
    ( 2013-05) Berumen, Michael L. ; Hoey, Andrew S. ; Bass, W. H. ; Bouwmeester, J. ; Catania, D. ; Cochran, Jesse E. M. ; Khalil, M. T. ; Miyake, S. ; Mughal, M. R. ; Spaet, J. L. Y. ; Saenz-Agudelo, Pablo
    The Red Sea has long been recognized as a region of high biodiversity and endemism. Despite this diversity and early history of scientific work, our understanding of the ecology of coral reefs in the Red Sea has lagged behind that of other large coral reef systems. We carried out a quantitative assessment of ISI-listed research published from the Red Sea in eight specific topics (apex predators, connectivity, coral bleaching, coral reproductive biology, herbivory, marine protected areas, non-coral invertebrates and reef associated bacteria) and compared the amount of research conducted in the Red Sea to that of the Australia’s Great Barrier Reef (GBR) and the Caribbean. On average, for these eight topics, the Red Sea had 1/6th the amount of research compared to the GBR and about 1/8th the amount of the Caribbean. Further, more than 50% of the published research from the Red Sea originated from the Gulf of Aqaba, a small area (< 2% of the area of the Red Sea) in the far northern Red Sea. We summarize the general state of knowledge in these eight topics and highlight areas of future research priorities for the Red Sea region. Notably, data that could inform science-based management approaches is badly lacking in most Red Sea countries. The Red Sea, as a geologically “young” sea located in one of the warmest regions of the world, has the potential to provide insight to pressing topics such as speciation processes as well as the capacity of reef systems and organisms to adapt to global climate change. As one of the world’s most biodiverse coral reef regions, the Red Sea may yet have a significant role to play in our understanding of coral reef ecology at a global scale.