Showing papers by "Robert J. Toonen published in 2019"

The molecular biogeography of the Indo-Pacific: testing hypotheses with multispecies genetic patterns

Abstract: Aim: To test hypothesized biogeographic partitions of the tropical Indo-Pacific Ocean with phylogeographic data from 56 taxa, and to evaluate the strength and nature of barriers emerging from this test. Location: The Indo-Pacific Ocean. Time period: Pliocene through the Holocene. Major taxa studied: Fifty-six marine species. Methods: We tested eight biogeographic hypotheses for partitioning of the Indo-Pacific using a novel modification to analysis of molecular variance. Putative barriers to gene flow emerging from this analysis were evaluated for pairwise ΦST, and these ΦST distributions were compared to distributions from randomized datasets and simple coalescent simulations of vicariance arising from the Last Glacial Maximum. We then weighed the relative contribution of distance versus environmental or geographic barriers to pairwise ΦST with a distance-based redundancy analysis (dbRDA). Results: We observed a diversity of outcomes, although the majority of species fit a few broad biogeographic regions. Repeated coalescent simulation of a simple vicariance model yielded a wide distribution of pairwise ΦST that was very similar to empirical distributions observed across five putative barriers to gene flow. Three of these barriers had median ΦST that were significantly larger than random expectation. Only 21 of 52 species analysed with dbRDA rejected the null model. Among these, 15 had overwater distance as a significant predictor of pairwise ΦST, while 11 were significant for geographic or environmental barriers other than distance. Main conclusions: Although there is support for three previously described barriers, phylogeographic discordance in the Indo-Pacific Ocean indicates incongruity between processes shaping the distributions of diversity at the species and population levels. Among the many possible causes of this incongruity, genetic drift provides the most compelling explanation: given massive effective population sizes of Indo-Pacific species, even hard vicariance for tens of thousands of years can yield ΦSTvalues that range from 0 to nearly 0.5.

Adaptive responses and local stressor mitigation drive coral resilience in warmer, more acidic oceans.

Abstract: Coral reefs have great biological and socioeconomic value, but are threatened by ocean acidification, climate change and local human impacts. The capacity for corals to adapt or acclimatize to nove...

High heritability of coral calcification rates and evolutionary potential under ocean acidification.

Abstract: Estimates of heritability inform evolutionary potential and the likely outcome of many management actions, but such estimates remain scarce for marine organisms. Here, we report high heritability of calcification rate among the eight most dominant Hawaiian coral species under reduced pH simulating future ocean conditions. Coral colonies were sampled from up to six locations across a natural mosaic in seawater chemistry throughout Hawaiʻi and fragmented into clonal replicates maintained under both ambient and high pCO2 conditions. Broad sense heritability of calcification rates was high among all eight species, ranging from a low of 0.32 in Porites evermanni to a high of 0.61 in Porites compressa. The overall results were inconsistent with short-term acclimatization to the local environment or adaptation to the mean or ideal conditions. Similarly, in ‘local vs. foreign’ and ‘home vs. away’ tests there was no clear signature of local adaptation. Instead, the data are most consistent with a protected polymorphism as the mechanism which maintains differential pH tolerance within the populations. Substantial individual variation, coupled with high heritability and large population sizes, imply considerable scope for natural selection and adaptive capacity, which has major implications for evolutionary potential and management of corals in response to climate change.

Shared genomic outliers across two divergent population clusters of a highly threatened seagrass.

Abstract: CITATION: Phair, N. L., et al. 2019. Shared genomic outliers across two divergent population clusters of a highly threatened seagrass. PeerJ, 7:e6806, doi:10.7717/peerj.6806.

Diversity and Structure of Parrotfish Assemblages across the Northern Great Barrier Reef

Abstract: The structure and dynamics of coral reef environments vary across a range of spatial scales, with patterns of associated faunal assemblages often reflecting this variability. However, delineating drivers of biological variability in such complex environments has proved challenging. Here, we investigated the assemblage structure and diversity of parrotfishes—a common and ecologically important group—across 6° of latitude on the Northern Great Barrier Reef (GBR), Australia. Parrotfish abundance and biomass were determined from stereo-video surveys across 82 sites spanning 31 reefs and assessed against geographic, biophysical, and management-related factors in a multivariate framework to determine major drivers and associated scales of assemblage structure. Large cross-shelf variation in parrotfish assemblages pervaded along the entire Northern GBR, with distinct assemblages associated with sheltered and exposed reefs. Species abundances and diversity generally decreased with decreasing latitude. The gradient of explicit predator biomass associated with management zoning had no effect on parrotfish assemblage structure, but was positively correlated with parrotfish diversity. Our results highlight the ubiquitous presence of cross-shelf variation, where the greatest differences in parrotfish community composition existed between sheltered (inner and mid shelf) and exposed (outer shelf) reef systems. Prior attempts to explain linkages between parrotfishes and fine-scale biophysical factors have demonstrated parrotfishes as habitat generalists, but recent developments in nutritional ecology suggest that their cross-shelf variation on the GBR is likely reflective of benthic resource distribution and species-specific feeding modes.

A coalescent sampler successfully detects biologically meaningful population structure overlooked by F-statistics.

Abstract: Assessing the geographic structure of populations has relied heavily on Sewell Wright's F-statistics and their numerous analogues for many decades. However, it is well appreciated that, due to their nonlinear relationship with gene flow, F-statistics frequently fail to reject the null model of panmixia in species with relatively high levels of gene flow and large population sizes. Coalescent genealogy samplers instead allow a model-selection approach to the characterization of population structure, thereby providing the opportunity for stronger inference. Here, we validate the use of coalescent samplers in a high gene flow context using simulations of a stepping-stone model. In an example case study, we then re-analyze genetic datasets from 41 marine species sampled from throughout the Hawaiian archipelago using coalescent model selection. Due to the archipelago's linear nature, it is expected that most species will conform to some sort of stepping-stone model (leading to an expected pattern of isolation by distance), but F-statistics have only supported this inference in ~10% of these datasets. Our simulation analysis shows that a coalescent sampler can make a correct inference of stepping-stone gene flow in nearly 100% of cases where gene flow is ≤100 migrants per generation (equivalent to F ST = 0.002), while F-statistics had mixed results. Our re-analysis of empirical datasets found that nearly 70% of datasets with an unambiguous result fit a stepping-stone model with varying population sizes and rates of gene flow, although 37% of datasets yielded ambiguous results. Together, our results demonstrate that coalescent samplers hold great promise for detecting weak but meaningful population structure, and defining appropriate management units.

Rare coral under the genomic microscope: timing and relationships among Hawaiian Montipora

Abstract: Evolutionary patterns of scleractinian (stony) corals are difficult to infer given the existence of few diagnostic characters and pervasive phenotypic plasticity. A previous study of Hawaiian Montipora (Scleractinia: Acroporidae) based on five partial mitochondrial and two nuclear genes revealed the existence of a species complex, grouping one of the rarest known species (M. dilatata, which is listed as Endangered by the International Union for Conservation of Nature - IUCN) with widespread corals of very different colony growth forms (M. flabellata and M. cf. turgescens). These previous results could result from a lack of resolution due to a limited number of markers, compositional heterogeneity or reflect biological processes such as incomplete lineage sorting (ILS) or introgression. All 13 mitochondrial protein-coding genes from 55 scleractinians (14 lineages from this study) were used to evaluate if a recent origin of the M. dilatata species complex or rate heterogeneity could be compromising phylogenetic inference. Rate heterogeneity detected in the mitochondrial data set seems to have no significant impacts on the phylogenies but clearly affects age estimates. Dating analyses show different estimations for the speciation of M. dilatata species complex depending on whether taking compositional heterogeneity into account (0.8 [0.05–2.6] Myr) or assuming rate homogeneity (0.4 [0.14–0.75] Myr). Genomic data also provided evidence of introgression among all analysed samples of the complex. RADseq data indicated that M. capitata colour morphs may have a genetic basis. Despite the volume of data (over 60,000 SNPs), phylogenetic relationships within the M. dilatata species complex remain unresolved most likely due to a recent origin and ongoing introgression. Species delimitation with genomic data is not concordant with the current taxonomy, which does not reflect the true diversity of this group. Nominal species within the complex are either undergoing a speciation process or represent ecomorphs exhibiting phenotypic polymorphisms.

RADseq population genomics confirms divergence across closely related species in blue coral (Heliopora coerulea).

Abstract: Heliopora coerulea, the blue coral, is the octocoral characterized by its blue skeleton. Recently, two Heliopora species were delimited by DNA markers: HC-A and HC-B. To clarify the genomic divergence of these Heliopora species (HC-A and HC-B) from sympatric and allopatric populations in Okinawa, Japan, we used a high throughput reduced representation genomic DNA sequencing approach (ezRAD). We found 6742 biallelic SNPs shared among all target populations, which successfully distinguished the HC-A and HC-B species in both the sympatric and allopatric populations, with no evidence of hybridization between the two. In addition, we detected 410 fixed SNPs linking functional gene differences, including heat resilience and reproductive timing, between HC-A and HC-B. We confirmed clear genomic divergence between Heliopora species and found possible genes related to stress-responses and reproduction, which may shed light on the speciation process and ecological divergence of coral species.

Evidence of local adaptation in a waterfall-climbing Hawaiian goby fish derived from coupled biophysical modeling of larval dispersal and post-settlement selection

Abstract: Local adaptation of marine and diadromous species is thought to be a product of larval dispersal, settlement mortality, and differential reproductive success, particularly in heterogeneous post-settlement habitats. We evaluated this premise with an oceanographic passive larval dispersal model coupled with individual-based models of post-settlement selection and reproduction to infer conditions that underlie local adaptation in Sicyopterus stimpsoni, an amphidromous Hawaiian goby known for its ability to climb waterfalls. Our model results demonstrated that larval dispersal is spatio-temporally asymmetric, with more larvae dispersed from the southeast (the Big Island) to northwest (Kaua‘i) along the archipelago, reflecting prevailing conditions such as El Nino/La Nina oscillations. Yet connectivity is nonetheless sufficient to result in homogenous populations across the archipelago. We also found, however, that ontogenetic shifts in habitat can give rise to adaptive morphological divergence when the strength of predation-driven post-settlement selection crosses a critical threshold. Notably, our simulations showed that larval dispersal is not the only factor determining the likelihood of morphological divergence. We found adaptive potential and evolutionary trajectories of S. stimpsoni were greater on islands with stronger environmental gradients and greater variance in larval cohort morphology due to fluctuating immigration. Contrary to expectation, these findings indicate that immigration can act in concert with selection to favor local adaptation and divergence in species with marine larval dispersal. Further development of model simulations, parameterized to reflect additional empirical estimates of abiotic and biotic factors, will help advance our understanding of the proximate and ultimate mechanisms driving adaptive evolution, population resilience, and speciation in marine-associated species.

Present-Day Distribution and Potential Spread of the Invasive Green Alga Avrainvillea amadelpha Around the Main Hawaiian Islands

Abstract: Algal assemblages are critical components of marine ecosystems from the intertidal to mesophotic depths; they act as primary producers, nutrient cyclers, and substrate providers. Coral reef ecosystems can be disrupted by stressors such as storm events, effluent inundation, sudden temperature shifts, and non-native invaders. Avrainvillea amadelpha is an invasive green alga that was first recorded in the main Hawaiian Islands on the west shore of Oahu and has continued to be of concern due to its extreme competitiveness with native algae and seagrasses. It has spread rapidly across the island of Oahu, decreasing the biodiversity of the benthos from shorelines to ~90 m depth. We employed a boosted regression tree modeling framework to identify highly vulnerable regions prone to invasion. Our model indicated that regions exposed to minimal bottom currents and at least five degree heating weeks are particularly susceptible to A. amadelpha colonization. Additionally, we extrapolated our model to the main Hawaiian Islands and forecasted how a 25% increase in statewide annual maximum degree heating weeks may change habitat suitability for A. amadelpha. Across all islands, we identified particularly vulnerable “hotspot” regions of concern for resource managers and conservationists. This manuscript demonstrates the utility of this approach for identifying priority regions for invasive species management in the face of a changing climate.

Molecular and morphological congruence of three new cryptic Neopetrosia spp. in the Caribbean.

Abstract: Neopetrosia proxima (Porifera: Demospongiae: Haplosclerida) is described as a morphologically variable sponge common on shallow reefs of the Caribbean. However, the range of morphological and reproductive variation within putative N. proxima led us to hypothesize that such variability may be indicative of cryptic species rather than plasticity. Using DNA sequences and morphological characters we confirmed the presence of three previously undescribed species of Neopetrosia. Morphological differences of each new congener were best resolved by partial gene sequences of the mitochondrial cytochrome oxidase subunit 1 over nuclear ones (18S rRNA and 28S rRNA). Several new characters for Neopetrosia were revealed by each new species. For example, N. dendrocrevacea sp. nov. and N. cristata sp. nov. showed the presence of grooves on the surface of the sponge body that converge at the oscula, and a more disorganized skeleton than previously defined for the genus. N. sigmafera sp. nov. adds the (1) presence of sigma microscleres, (2) significantly wider/longer oxeas (>200 μm), and (3) the presence of parenchymella larvae. Sampling of conspecifics throughout several locations in the Caribbean revealed larger spicules in habitats closer to the continental shelf than those in remote island locations. Our study highlights the importance of integrating molecular and morphological systematics for the discrimination of new Neopetrosia spp. despite belonging to one of several polyphyletic groups (families, genera) within the current definition of the order Haplosclerida.

The Hawaiian Archipelago

Abstract: The Hawaiian Archipelago is one of the largest and most isolated island chains in the world, and its marine ecosystems are well-studied. Research on Hawaiian mesophotic coral ecosystems (MCEs) began in the 1960s and has intensified during the past decade. In Hawai‘i, rich communities of macroalgae, corals and other invertebrates, and fishes inhabit MCEs and are associated with increased water clarity and decreasing average current strength with depth. Extensive calcified and fleshy macroalgal beds are found both in discrete patches, dense beds, and meadows over both hard and soft substrates. Several species of corals typical of shallow reefs extend to depths of ~60 m. The dominant corals below 60 m are in the genus Leptoseris, which can form extensive coral reefs spanning tens of km2. Few octocoral species inhabit shallow reefs and upper MCEs (30–70 m) but are diverse at the deepest range of MCEs (>130 m). Sponges do not represent a major structural component of MCEs. Many species of fishes occur on both shallow reefs and MCEs, but MCEs harbor more endemic species (up to 100% endemism). Several new species of macroalgae, corals and other invertebrates, and fishes have recently been documented. Over 60% of the territorial waters surrounding the archipelago are protected as the Papahānaumokuākea Marine National Monument; however, no specific protections exist for MCEs. Generally, threats affecting Hawai‘i’s shallow reefs also affect MCEs to varying degrees. MCEs may be more insulated from some threats but more vulnerable than shallow reefs to others (e.g., water clarity).

Annotated checklist for stony corals of American Sāmoa with reference to mesophotic depth records

Abstract: An annotated checklist of the stony corals (Scleractinia, Milleporidae, Stylasteridae, and Helioporidae) of American Sāmoa is presented. A total of 377 valid species has been reported from American Sāmoa with 342 species considered either present (251) or possibly present (91). Of these 342 species, 66 have a recorded geographical range extension and 90 have been reported from mesophotic depths (30-150 m). Additionally, four new species records (Acanthastreasubechinata Veron, 2000, Favitesparaflexuosus Veron, 2000, Echinophylliaechinoporoides Veron & Pichon, 1980, Turbinariairregularis Bernard, 1896) are presented. Coral species of concern include species listed under the US Endangered Species Act (ESA) and the International Union for Conservation of Nature's (IUCN) Red List of threatened species. Approximately 17.5% of the species present or possibly present are categorized as threatened by IUCN compared to 27% of the species globally. American Sāmoa has seven ESA-listed or ESA candidate species, including Acroporaglobiceps (Dana, 1846), Acroporajacquelineae Wallace, 1994, Acroporaretusa (Dana, 1846), Acroporaspeciosa (Quelch, 1886), Fimbriaphylliaparadivisa (Veron, 1990), Isoporacrateriformis (Gardiner, 1898), and Pocilloporameandrina Dana, 1846. There are two additional species possibly present, i.e., Pavonadiffluens (Lamarck, 1816) and Poritesnapopora Veron, 2000.

Genetic structure is stronger across human-impacted habitats than among islands in the coral Porites lobata

Abstract: We examined genetic structure in the lobe coral Porites lobata among pairs of highly variable and high-stress nearshore sites and adjacent less variable and less impacted offshore sites on the islands of Oahu and Maui, Hawai i. Using an analysis of molecular variance framework, we tested whether populations were more structured by geographic distance or environmental extremes. The genetic patterns we observed followed isolation by environment, where nearshore and adjacent offshore populations showed significant genetic structure at both locations (AMOVA FST = 0.04 [~] 0.19, P < 0.001), but no significant isolation by distance between islands. In contrast, a third site with a less impacted nearshore site showed no significant structure. Strikingly, corals from the two impacted nearshore sites on different islands over 100km apart with similar environmentally stressful conditions were genetically closer (FST[~] 0, P = 0.733) than those within a single location less than 2 km apart (FST= 0.041[~]0.079, P < 0.01). Our results suggest that ecological boundaries appear to play a strong role in forming genetic structure in the coastal environment, and that genetic divergence in the absence of geographical barriers to gene flow may be explained by disruptive selection across contrasting habitats.

A behavioral and genetic study of multiple paternity in a polygamous marine invertebrate, Octopus oliveri.

Abstract: Octopus oliveri is a widespread and common rocky intertidal cephalopod that mates readily in the laboratory, but for which mating behavior has not been reported previously. Four sets of behavioral experiments were recorded wherein three males, small, medium & large in varying order, were introduced to each of six females, for a total of 24 individual females and 12 individual males utilized in the experiments. Video analysis shows that successful mating occurred in each of the mount, reach and beak-to-beak positions. Mating was observed for all males, regardless of size relative to the female, or order of introduction. Females showed preference for the first male to which they were introduced in experimental pairings rather than any specific male trait, and mating time increased significantly with increasing female size. Five novel microsatellite markers were developed and used to test paternity in the eleven broods resulting from these experimental pairings. We found skewed paternity in each brood, with early male precedence and male size being the best predictors of parentage. Multiple paternity was observed in every experimental cross but was estimated to be comparatively low in the field, suggesting that sperm limitation might be common in this species. We saw no evidence of direct sperm competition in Octopus oliveri, but larger males produced significantly more offspring. This study contributes to the growing research on cephalopod mating systems and indicates that octopus mating dynamics might be more variable and complex than thought previously.

Re-description of type material of Xenia Lamarck, 1816 (Octocorallia: Xeniidae).

Abstract: In this study we examined the original types of 21 of the 56 morphospecies of Xenia currently listed in WoRMS. Unfortunately, our attempts to locate additional type material failed, and we conclude that they have been lost. The type localities of the material examined include the Red Sea, West and Central Indian Ocean, the South Pacific, Indonesia, The Philippines, and the Bismarck Sea, reflecting the extensive biogeographical distribution of this genus throughout the Indo-Pacific Ocean. A neotype was designated from the northern Red Sea for X. umbellata, and sequencing established its position in the phylogenetic tree in relation to other genera of the family Xeniidae. In addition, X. flexibilis n. sp. was described from The Philippines. The findings from the current study led to the synonymizing of X. actuosa with X. sansibariana and of X. plicata with X. blumi. Overall, the study has re-described the types of 17 species considered to be valid based on morphological characters. Validation of the morphological features of original type material along with species-diagnostic genetic characters are required in order to facilitate our ability to correctly employ Latin binomials, both in phylogenetic studies and in any other biological surveys.

The complete mitochondrial genome of the Band-rumped Storm Petrel (Oceanodroma castro)

Abstract: In this study, we report the complete mitochondrial genome sequence of the Endangered Band-rumped Storm Petrel (Oceanodroma castro), a globally distributed seabird. The mitogenome is 17,023 bp in l...