Eric D. Crandall

Comparative Phylogeography of the Coral Triangle and Implications for Marine Management

Extreme concentration of marine biodiversity and exploitation of marine resources in the Coral Triangle pose challenges to biogeographers and resource managers. Comparative phylogeography provides a powerful tool to test biogeographic hypotheses evoked to explain species richness in the Coral Triangle. It can also be used to delineate management units for marine resources. After about a decade of phylogeographical studies, patterns for the Coral Triangle are emerging. Broad connectivity in some species support the notion that larvae have maintained gene flow among distant populations for long periods. Other phylogeographic patterns suggest vicariant events resulting from Pleistocene sea level fluctuations, which have, at least occasionally, resulted in speciation. Divergence dates ranging back to the Miocene suggest that changing land configurations may have precipitated an explosion of species diversification. A synthesis of the marine phylogeographic studies reveals repeated patterns that corroborate hypothesized biogeographic processes and suggest improved management schemes for marine resources.

Contrasting demographic history and phylogeographical patterns in two Indo-Pacific gastropods

Marine species with ranges that span the Indo‐Australian Archipelago (IAA) exhibit a range of phylogeographical patterns, most of which are interpreted in the context of vicariance between Indian and Pacific Ocean populations during Pliocene and Pleistocene low sea‐level stands. However, patterns often vary among ecologically similar taxa, sometimes even within genera. This study compares phylogeographical patterns in two species of highly dispersive neritid gastropod, Nerita albicilla and Nerita plicata, with nearly sympatric ranges that span the Indo‐Pacific. Mitochondrial COI sequences from > 1000 individuals from 97 sites reveal similar phylogenies in both species (two divergent clades differing by 3.2% and 2.3%, for N. albicilla and N. plicata, respectively). However, despite ecological similarity and congeneric status, the two species exhibit phylogeographical discordance. N. albicilla has maintained reciprocal monophyly of Indian and Pacific Ocean populations, while N. plicata is panmictic between oceans, but displays a genetic cline in the Central Pacific. Although this difference might be explained by qualitatively different demographic histories, parameter estimates from three coalescent models indicate that both species have high levels of gene flow between demes (2Nem > 75), and share a common history of population expansion that is likely associated with cyclical flooding of continental shelves and island lagoons following low sea‐level stands. Results indicate that ecologically similar, codistributed species may respond very differently to shared environmental processes, suggesting that relatively minor differences in traits such as pelagic larval duration or microhabitat association may profoundly impact phylogeographical structure.

Comparative phylogeography of two seastars and their ectosymbionts within the Coral Triangle

Repeated exposure and flooding of the Sunda and Sahul shelves during Pleistocene sea‐level fluctuations is thought to have contributed to the isolation and diversification of sea‐basin populations within the Coral Triangle. This hypothesis has been tested in numerous phylogeographical studies, recovering an assortment of genetic patterns that the authors have generally attributed to differences in larval dispersal capability or adult habitat specificity. This study compares phylogeographical patterns from mitochondrial COI sequences among two co‐distributed seastars that differ in their adult habitat and dispersal ability, and two seastar ectosymbionts that differ in their degree of host specificity. Of these, only the seastar Linckia laevigata displayed a classical pattern of Indian‐Pacific divergence, but with only moderate genetic structure (ΦCT = 0.067). In contrast, the seastar Protoreaster nodosus exhibited strong structure (ΦCT = 0.23) between Teluk Cenderawasih and the remainder of Indonesia, a pattern of regional structure that was echoed in L. laevigata (ΦCT = 0.03) as well as its obligate gastropod parasite Thyca crystallina (ΦCT = 0.04). The generalist commensal shrimp, Periclimenes soror showed little genetic structuring across the Coral Triangle. Despite species‐specific phylogeographical patterns, all four species showed departures from neutrality that are consistent with massive range expansions onto the continental shelves as the sea levels rose, and that date within the Pleistocene epoch. Our results suggest that habitat differences may affect the manner in which species responded to Pleistocene sea‐level fluctuations, shaping contemporary patterns of genetic structure and diversity.

Expansion Dating: Calibrating Molecular Clocks in Marine Species from Expansions onto the Sunda Shelf Following the Last Glacial Maximum

The rate of change in DNA is an important parameter for understanding molecular evolution and hence for inferences drawn from studies of phylogeography and phylogenetics. Most rate calibrations for mitochondrial coding regions in marine species have been made from divergence dating for fossils and vicariant events older than 1-2 My and are typically 0.5-2% per lineage per million years. Recently, calibrations made with ancient DNA (aDNA) from younger dates have yielded faster rates, suggesting that estimates of the molecular rate of change depend on the time of calibration, decaying from the instantaneous mutation rate to the phylogenetic substitution rate. aDNA methods for recent calibrations are not available for most marine taxa so instead we use radiometric dates for sea-level rise onto the Sunda Shelf following the Last Glacial Maximum (starting ∼18,000 years ago), which led to massive population expansions for marine species. Instead of divergence dating, we use a two-epoch coalescent model of logistic population growth preceded by a constant population size to infer a time in mutational units for the beginning of these expansion events. This model compares favorably to simpler coalescent models of constant population size, and exponential or logistic growth, and is far more precise than estimates from the mismatch distribution. Mean rates estimated with this method for mitochondrial coding genes in three invertebrate species are elevated in comparison to older calibration points (2.3-6.6% per lineage per million years), lending additional support to the hypothesis of calibration time dependency for molecular rates.

High gene flow due to pelagic larval dispersal among South Pacific archipelagos in two amphidromous gastropods (Neritomorpha: Neritidae).

The freshwater stream fauna of tropical oceanic islands is dominated by amphidromous species, whose larvae are transported to the ocean and develop in the plankton before recruiting back to freshwater habitat as juveniles. Because stream habitat is relatively scarce and unstable on oceanic islands, this life history would seem to favor either the retention of larvae to their natal streams, or the ability to delay metamorphosis until new habitat is encountered. To distinguish between these hypotheses, we used population genetic methods to estimate larval dispersal among five South Pacific archipelagos in two amphidromous species of Neritid gastropod (Neritina canalis and Neripteron dilatatus). Sequence data from mitochondrial cytochrome oxidase I (COI) revealed that neither species is genetically structured throughout the Western Pacific, suggesting that their larvae have a pelagic larval duration (PLD) of at least 8 weeks, longer than many marine species. In addition, the two species have recently colonized isolated Central Pacific archipelagos in three independent events. Since colonization, there has been little or no gene flow between the Western and Central Pacific archipelagos in N. canalis, and high levels of gene flow across the same region in N. dilatatus. Both species show departures from neutrality and recent dates for colonization of the Central Pacific archipelagos, which is consistent with frequent extinction and recolonization of stream populations in this area. Similar results from other amphidromous species suggest that unstable freshwater habitats promote long-distance dispersal capabilities.

Coalescent and Biophysical Models of Stepping-Stone Gene Flow in Neritid Snails

Marine species in the Indo‐Pacific have ranges that can span thousands of kilometres, yet studies increasingly suggest that mean larval dispersal distances are less than historically assumed. Gene flow across these ranges must therefore rely to some extent on larval dispersal among intermediate ‘stepping‐stone’ populations in combination with long‐distance dispersal far beyond the mean of the dispersal kernel. We evaluate the strength of stepping‐stone dynamics by employing a spatially explicit biophysical model of larval dispersal in the tropical Pacific to construct hypotheses for dispersal pathways. We evaluate these hypotheses with coalescent models of gene flow among high‐island archipelagos in four neritid gastropod species. Two of the species live in the marine intertidal, while the other two are amphidromous, living in fresh water but retaining pelagic dispersal. Dispersal pathways predicted by the biophysical model were strongly favoured in 16 of 18 tests against alternate hypotheses. In regions where connectivity among high‐island archipelagos was predicted as direct, there was no difference in gene flow between marine and amphidromous species. In regions where connectivity was predicted through stepping‐stone atolls only accessible to marine species, gene flow estimates between high‐island archipelagos were significantly higher in marine species. Moreover, one of the marine species showed a significant pattern of isolation by distance consistent with stepping‐stone dynamics. While our results support stepping‐stone dynamics in Indo‐Pacific species, we also see evidence for nonequilibrium processes such as range expansions or rare long‐distance dispersal events. This study couples population genetic and biophysical models to help to shed light on larval dispersal pathways.

Use of Genetic Stock Identification Data for Comparison of the Ocean Spatial Distribution, Size at Age, and Fishery Exposure of an Untagged Stock and Its Indicator: California Coastal versus Klamath River Chinook Salmon

AbstractManaging weak stocks in mixed-stock fisheries often relies on proxies derived from data-rich indicator stocks, although there have been limited tests of the appropriateness of such proxies. For example, full cohort reconstruction of tagged Klamath River fall-run Chinook Salmon Oncorhynchus tshawytscha of northern California enables the use of detailed models to inform management. Information gained from this stock is also used in the management of the untagged, threatened California Coastal Chinook Salmon (CCC) stock, where it is assumed that a cap on Klamath harvest rates effectively constrains impacts on CCC to acceptable levels. To evaluate use of this proxy, we used a novel approach based on genetic stock identification (GSI) data to compare the two stocks’ size at age and ocean distribution (as inferred from spatial variation in CPUE), two key factors influencing fishery exposure. We developed broadly applicable methods to account for both sampling and genetic assignment uncertainty in estima...

Navigating the currents of seascape genomics: how spatial analyses can augment population genomic studies

Population genomic approaches are making rapid inroads in the study of non-model organisms, including marine taxa. To date, these marine studies have predominantly focused on rudimentary metrics describing the spatial and environmental context of their study region (e.g., geographical distance, average sea surface temperature, average salinity). We contend that a more nuanced and considered approach to quantifying seascape dynamics and patterns can strengthen population genomic investigations and help identify spatial, temporal, and environmental factors associated with differing selective regimes or demographic histories. Nevertheless, approaches for quantifying marine landscapes are complicated. Characteristic features of the marine environment, including pelagic living in flowing water (experienced by most marine taxa at some point in their life cycle), require a well-designed spatial-temporal sampling strategy and analysis. Many genetic summary statistics used to describe populations may be inappropriate for marine species with large population sizes, large species ranges, stochastic recruitment, and asymmetrical gene flow. Finally, statistical approaches for testing associations between seascapes and population genomic patterns are still maturing with no single approach able to capture all relevant considerations. None of these issues are completely unique to marine systems and therefore similar issues and solutions will be shared for many organisms regardless of habitat. Here, we outline goals and spatial approaches for landscape genomics with an emphasis on marine systems and review the growing empirical literature on seascape genomics. We review established tools and approaches and highlight promising new strategies to overcome select issues including a strategy to spatially optimize sampling. Despite the many challenges, we argue that marine systems may be especially well suited for identifying candidate genomic regions under environmentally mediated selection and that seascape genomic approaches are especially useful for identifying robust locus-by-environment associations.

Geo-Referenced, Abundance Calibrated Ocean Distribution of Chinook Salmon ( Oncorhynchus tshawytscha ) Stocks across the West Coast of North America

Understanding seasonal migration and localized persistence of populations is critical for effective species harvest and conservation management. Pacific salmon (genus Oncorhynchus) forecasting models predict stock composition, abundance, and distribution during annual assessments of proposed fisheries impacts. Most models, however, fail to account for the influence of biophysical factors on year-to-year fluctuations in migratory distributions and stock-specific survival. In this study, the ocean distribution and relative abundance of Chinook salmon (O. tshawytscha) stocks encountered in the California Current large marine ecosystem, U.S.A were inferred using catch-per-unit effort (CPUE) fisheries and genetic stock identification data. In contrast to stock distributions estimated through coded-wire-tag recoveries (typically limited to hatchery salmon), stock-specific CPUE provides information for both wild and hatchery fish. Furthermore, in contrast to stock composition results, the stock-specific CPUE metric is independent of other stocks and is easily interpreted over multiple temporal or spatial scales. Tests for correlations between stock-specific CPUE and stock composition estimates revealed these measures diverged once proportional contributions of locally rare stocks were excluded from data sets. A novel aspect of this study was collection of data both in areas closed to commercial fisheries and during normal, open commercial fisheries. Because fishing fleet efficiency influences catch rates, we tested whether CPUE differed between closed area (non-retention) and open area (retention) data sets. A weak effect was indicated for some, but not all, analyzed cases. Novel visualizations produced from stock-specific CPUE-based ocean abundance facilitates consideration of how highly refined, spatial and genetic information could be incorporated in ocean fisheries management systems and for investigations of biogeographic factors that influence migratory distributions of fish.

The Genomic Observatories Metadatabase (GeOMe): a new repository for field and sampling event metadata associated with genetic samples

The Genomic Observatories Metadatabase (GeOMe, http://www.geome-db.org/) is an open access repository for geographic and ecological metadata associated with biosamples and genetic data. Whereas public databases have served as vital repositories for nucleotide sequences, they do not accession all the metadata required for ecological or evolutionary analyses. GeOMe fills this need, providing a user-friendly, web-based interface for both data contributors and data recipients. The interface allows data contributors to create a customized yet standard-compliant spreadsheet that captures the temporal and geospatial context of each biosample. These metadata are then validated and permanently linked to archived genetic data stored in the National Center for Biotechnology Information’s (NCBI’s) Sequence Read Archive (SRA) via unique persistent identifiers. By linking ecologically and evolutionarily relevant metadata with publicly archived sequence data in a structured manner, GeOMe sets a gold standard for data management in biodiversity science.