Michelle R. Gaither

Phylogeography of the reef fish Cephalopholis argus(Epinephelidae) indicates Pleistocene isolation across the indo-pacific barrier with contemporary overlap in the coral triangle

BackgroundThe Coral Triangle (CT), bounded by the Philippines, the Malay Peninsula, and New Guinea, is the epicenter of marine biodiversity. Hypotheses that explain the source of this rich biodiversity include 1) the center of origin, 2) the center of accumulation, and 3) the region of overlap. Here we contribute to the debate with a phylogeographic survey of a widely distributed reef fish, the Peacock Grouper (Cephalopholis argus; Epinephelidae) at 21 locations (N = 550) using DNA sequence data from mtDNA cytochrome b and two nuclear introns (gonadotropin-releasing hormone and S7 ribosomal protein).ResultsPopulation structure was significant (ΦST = 0.297, P < 0.001; FST = 0.078, P < 0.001; FST = 0.099, P < 0.001 for the three loci, respectively) among five regions: French Polynesia, the central-west Pacific (Line Islands to northeastern Australia), Indo-Pacific boundary (Bali and Rowley Shoals), eastern Indian Ocean (Cocos/Keeling and Christmas Island), and western Indian Ocean (Diego Garcia, Oman, and Seychelles). A strong signal of isolation by distance was detected in both mtDNA (r = 0.749, P = 0.001) and the combined nuclear loci (r = 0.715, P < 0.001). We detected evidence of population expansion with migration toward the CT. Two clusters of haplotypes were detected in the mtDNA data (d = 0.008), corresponding to the Pacific and Indian Oceans, with a low level of introgression observed outside a mixing zone at the Pacific-Indian boundary.ConclusionsWe conclude that the Indo-Pacific Barrier, operating during low sea level associated with glaciation, defines the primary phylogeographic pattern in this species. These data support a scenario of isolation on the scale of 105 year glacial cycles, followed by population expansion toward the CT, and overlap of divergent lineages at the Pacific-Indian boundary. This pattern of isolation, divergence, and subsequent overlap likely contributes to species richness at the adjacent CT and is consistent with the region of overlap hypothesis.

Defining Boundaries for Ecosystem-Based Management: A Multispecies Case Study of Marine Connectivity across the Hawaiian Archipelago.

Determining the geographic scale at which to apply ecosystem-based management (EBM) has proven to be an obstacle for many marine conservation programs. Generalizations based on geographic proximity, taxonomy, or life history characteristics provide little predictive power in determining overall patterns of connectivity, and therefore offer little in terms of delineating boundaries for marine spatial management areas. Here, we provide a case study of 27 taxonomically and ecologically diverse species (including reef fishes, marine mammals, gastropods, echinoderms, cnidarians, crustaceans, and an elasmobranch) that reveal four concordant barriers to dispersal within the Hawaiian Archipelago which are not detected in single-species exemplar studies. We contend that this multispecies approach to determine concordant patterns of connectivity is an objective and logical way in which to define the minimum number of management units and that EBM in the Hawaiian Archipelago requires at least five spatially managed regions.

Comparative phylogeography of the ocean planet.

Understanding how geography, oceanography, and climate have ultimately shaped marine biodiversity requires aligning the distributions of genetic diversity across multiple taxa. Here, we examine phylogeographic partitions in the sea against a backdrop of biogeographic provinces defined by taxonomy, endemism, and species composition. The taxonomic identities used to define biogeographic provinces are routinely accompanied by diagnostic genetic differences between sister species, indicating interspecific concordance between biogeography and phylogeography. In cases where individual species are distributed across two or more biogeographic provinces, shifts in genotype frequencies often align with biogeographic boundaries, providing intraspecific concordance between biogeography and phylogeography. Here, we provide examples of comparative phylogeography from (i) tropical seas that host the highest marine biodiversity, (ii) temperate seas with high productivity but volatile coastlines, (iii) migratory marine fauna, and (iv) plankton that are the most abundant eukaryotes on earth. Tropical and temperate zones both show impacts of glacial cycles, the former primarily through changing sea levels, and the latter through coastal habitat disruption. The general concordance between biogeography and phylogeography indicates that the population-level genetic divergences observed between provinces are a starting point for macroevolutionary divergences between species. However, isolation between provinces does not account for all marine biodiversity; the remainder arises through alternative pathways, such as ecological speciation and parapatric (semiisolated) divergences within provinces and biodiversity hotspots.

Genomic signatures of geographic isolation and natural selection in coral reef fishes

The drivers of speciation remain among the most controversial topics in evolutionary biology. Initially, Darwin emphasized natural selection as a primary mechanism of speciation, but the architects of the modern synthesis largely abandoned that view in favour of divergence by geographic isolation. The balance between selection and isolation is still at the forefront of the evolutionary debate, especially for the worlds tropical oceans where biodiversity is high, but isolating barriers are few. Here, we identify the drivers of speciation in Pacific reef fishes of the genus Acanthurus by comparative genome scans of two peripheral populations that split from a large Central‐West Pacific lineage at roughly the same time. Mitochondrial sequences indicate that populations in the Hawaiian Archipelago and the Marquesas Islands became isolated approximately 0.5 Ma. The Hawaiian lineage is morphologically indistinguishable from the widespread Pacific form, but the Marquesan form is recognized as a distinct species that occupies an unusual tropical ecosystem characterized by upwelling, turbidity, temperature fluctuations, algal blooms and little coral cover. An analysis of 3737 SNPs reveals a strong signal of selection at the Marquesas, with 59 loci under disruptive selection including an opsin Rh2 locus. While both the Hawaiian and Marquesan populations indicate signals of drift, the former shows a weak signal of selection that is comparable with populations in the Central‐West Pacific. This contrast between closely related lineages reveals one population diverging due primarily to geographic isolation and genetic drift, and the other achieving taxonomic species status under the influence of selection.

Evolution of pygmy angelfishes: Recent divergences, introgression, and the usefulness of color in taxonomy

The pygmy angelfishes (genus Centropyge, family Pomacanthidae) are brightly colored species that occupy reef habitats in every tropical ocean. Some species are rarely observed because they occur below conventional scuba depths. Their striking coloration can command thousands of U.S. dollars in the aquarium trade, and closely related species are often distinguished only by coloration. These factors have impeded phylogenetic resolution, and every phylogeographic survey to date has reported discordance between coloration, taxonomy, and genetic partitions. Here we report a phylogenetic survey of 29 of the 34 recognized species (N=94 plus 23 outgroups), based on two mtDNA and three nuclear loci, totaling 2272 bp. The resulting ML and Baysian trees are highly concordant and indicate that the genus Centropyge is paraphyletic, consistent with a previous analysis of the family Pomacanthidae. Two recognized genera (Apolemichthys and Genicanthus) nest within Centropyge, and two subgenera (Xiphypops and Paracentropyge) comprise monophyletic lineages that should be elevated to genus level. Based on an age estimate of 38 Ma for the family Pomacanthidae, Centropyge diverged from the closest extant genus Pygoplites about 33 Ma, three deep lineages within Centropyge diverged about 18-28 Ma, and four species complexes diverged 3-12 Ma. However, in 11 of 13 cases, putative species in these complexes are indistinguishable based on morphology and genetics, being defined solely by coloration. These cases indicate either emerging species or excessive taxonomic splitting based on brightly colored variants.

Genetic consequences of introducing allopatric lineages of Bluestriped Snapper (Lutjanus kasmira) to Hawaii

A half century ago the State of Hawaii began a remarkable, if unintentional, experiment on the population genetics of introduced species, by releasing 2431 Bluestriped Snappers (Lutjanus kasmira) from the Marquesas Islands in 1958 and 728 conspecifics from the Society Islands in 1961. By 1992 L. kasmira had spread across the entire archipelago, including locations 2000 km from the release site. Genetic surveys of the source populations reveal diagnostic differences in the mtDNA control region (d = 3.8%; φST = 0.734, P < 0.001) and significant allele frequency differences at nuclear DNA loci (FST = 0.49; P < 0.001). These findings, which indicate that source populations have been isolated for approximately half a million years, set the stage for a survey of the Hawaiian Archipelago (N = 385) to determine the success of these introductions in terms of genetic diversity and breeding behaviour. Both Marquesas and Society mtDNA lineages were detected at each survey site across the Hawaiian Archipelago, at about the same proportion or slightly less than the original 3.4:1 introduction ratio. Nuclear allele frequencies and parentage tests demonstrate that the two source populations are freely interbreeding. The introduction of 2431 Marquesan founders produced only a slight reduction in mtDNA diversity (17%), while the 728 Society founders produced a greater reduction in haplotype diversity (41%). We find no evidence of genetic bottlenecks between islands of the Hawaiian Archipelago, as expected under a stepping‐stone model of colonization, from the initial introduction site. This species rapidly colonized across 2000 km without loss of genetic diversity, illustrating the consequences of introducing highly dispersive marine species.

Preservation of corals in salt-saturated DMSO buffer is superior to ethanol for PCR experiments

Specimen collection is time consuming and expensive, yet few laboratories test preservation methods before setting out on field expeditions. The most common preservation buffer used for coral specimens is >70% EtOH. However, alternatives exist that are less flammable, easier to ship, and are widely used in other taxa. Here, we compare the effects of salt-saturated DMSO (SSD) and EtOH preservation buffers on post-extraction DNA quantity and quality. We found that soft tissue integrity was better maintained and higher quantities of DNA were extracted from EtOH-preserved specimens; however, by all other measures, SSD was a superior preservative to EtOH. Extractions of SSD-preserved specimens resulted in higher molecular weight DNA, higher PCR success, and more efficient amplification than specimens preserved in EtOH. Our results show that SSD is generally a superior preservative to EtOH for specimens destined for PCR studies, but species-specific differences indicate that preservation comparisons should be undertaken before collection and storage of samples.

Seascape genetics along environmental gradients in the Arabian Peninsula: insights from ddRAD sequencing of anemonefishes

Understanding the processes that shape patterns of genetic structure across space is a central aim of landscape genetics. However, it remains unclear how geographical features and environmental variables shape gene flow, particularly for marine species in large complex seascapes. Here, we evaluated the genomic composition of the two‐band anemonefish Amphiprion bicinctus across its entire geographical range in the Red Sea and Gulf of Aden, as well as its close relative, Amphiprion omanensis endemic to the southern coast of Oman. Both the Red Sea and the Arabian Sea are complex and environmentally heterogeneous marine systems that provide an ideal scenario to address these questions. Our findings confirm the presence of two genetic clusters previously reported for A. bicinctus in the Red Sea. Genetic structure analyses suggest a complex seascape configuration, with evidence of both isolation by distance (IBD) and isolation by environment (IBE). In addition to IBD and IBE, genetic structure among sites was best explained when two barriers to gene flow were also accounted for. One of these coincides with a strong oligotrophic–eutrophic gradient at around 16–20˚N in the Red Sea. The other agrees with a historical bathymetric barrier at the straight of Bab al Mandab. Finally, these data support the presence of interspecific hybrids at an intermediate suture zone at Socotra and indicate complex patterns of genomic admixture in the Gulf of Aden with evidence of introgression between species. Our findings highlight the power of recent genomic approaches to resolve subtle patterns of gene flow in marine seascapes.

Population structure in the native range predicts the spread of introduced marine species

Forecasting invasion success remains a fundamental challenge in invasion biology. The effort to identify universal characteristics that predict which species become invasive has faltered in part because of the diversity of taxa and systems considered. Here, we use an alternative approach focused on the spread stage of invasions. FST, a measure of alternative fixation of alleles, is a common proxy for realized dispersal among natural populations, summarizing the combined influences of life history, behaviour, habitat requirements, population size, history and ecology. We test the hypothesis that population structure in the native range (FST) is negatively correlated with the geographical extent of spread of marine species in an introduced range. An analysis of the available data (29 species, nine phyla) revealed a significant negative correlation (R2 = 0.245–0.464) between FST and the extent of spread of non-native species. Mode FST among pairwise comparisons between populations in the native range demonstrated the highest predictive power (R2 = 0.464, p < 0.001). There was significant improvement when marker type was considered, with mtDNA datasets providing the strongest relationship (n = 21, R2 = 0.333–0.516). This study shows that FST can be used to make qualitative predictions concerning the geographical extent to which a non-native marine species will spread once established in a new area.

Long‐term sperm storage in the brownbanded bamboo shark Chiloscyllium punctatum

This study investigated the birth of a brownbanded bamboo shark Chiloscyllium punctatum at the Steinhart Aquarium. Genetic analyses suggest this is the longest documented case of sperm storage for any species of shark (45 months).