Magnificent dimensions, varied forms, and brilliant colors: The molecular ecology and evolution of the Indian and Pacific oceans

The tropical Indian and Pacific oceans form the world's largest and most speciose marine biogeographic region: the Indo-Pacific. Due to its size and political complexity, the Indo-Pacific is rarely studied as a whole, yet comprehensive studies of the region promise to teach us much about marine ecology and evolution. Molecular methods can provide substantial initial insights into the processes that create and maintain biodiversity in the region while also providing critical spatial information to managers. This special issue presents six synthetic papers that discuss the current state of molecular work in the Indo-Pacific region as well as best practices for the future. Following these synthetic papers are 15 empirical papers that extend our knowledge of the region considerably. A comprehensive understanding of the biodiversity that we stand to lose in the Indo-Pacific is going to require increased cooperation and collaboration among laboratories that study this region, as exemplified by papers in this special issue

Evaluating edge-of-range genetic patterns for tropical echinoderms, Acanthaster planci and Tripneustes gratilla, of the Kermadec Islands, southwest Pacific

Edge-of-range populations are often typified by patterns of low genetic diversity and high genetic differentiation relative to populations within the core of a species range. The "core-periphery hypothesis," also known as the "central-marginal hypothesis," predicts that these genetic patterns at the edge-of-range are a consequence of reduced population size and connectivity toward a species range periphery. It is unclear, however, how these expectations relate to high dispersal marine species that can conceivably maintain high abundance and high connectivity at their range edge. In the present study, we characterize the genetic patterns of two tropical echinoderm populations in the Kermadec Islands, the edge of their southwest Pacific range, and compare these genetic patterns to those from populations throughout their east Indian and Pacific ranges. We find that the populations of both Acanthaster planci (Linnaeus, 1758) and Tripneustes gratilla (Linnaeus, 1758) are represented by a single haplotype at the Kermadec Islands (based on mitochondrial cytochrome oxidase C subunit I). Such low genetic diversity concurs with the expectations of the "core-periphery hypothesis." Furthermore, the haplotypic composition of both populations suggests they have been founded by a small number of colonists with little subsequent immigration. Thus, local reproduction and self-recruitment appear to maintain these populations despite the ecologically marginal conditions of the Kermadec Islands for these tropical species. Understanding rates of self-recruitment vs reliance on connectivity with populations outside of the Kermadec Islands has implications for the persistence of these populations and range stability of these echinoderm species

Can sea snakes slither through seascape structure? Comparative phylogeography and population genetics of Hydrophis group sea snakes in Australia and Southeast Asia

Pleistocene sea level changes substantially shaped the biogeography of northern Australia and the Indo-Malayan Archipelago (IMA). For co-distributed species, their phylogeographic and population genetic patterns are expected to be concomitant with geological transformations of the Pleistocene. However, species-specific ecologies and life history traits may also be influential in generating patterns which depart from simple expectations arising from biogeographic features. Thus, comparative population genetic studies, which use taxa that reduces variation in taxonomy and geography, may refine our understanding of how biogeographic elements shape the populations of co-occurring species. Here, we sampled two sea snake species, Hydrophis curtus and H. elegans, throughout their known ranges in the IMA and northern Australia. These sea snakes have similar life history strategies and ecologies as well as overlapping distributions across the Torres Strait, a well-known biogeographic feature. We analysed two mitochondrial DNA (mtDNA) fragments and 10 microsatellite loci using traditional population genetic approaches and used Bayesian clustering methods to examine species- specific phylogenetic relationships, genetic diversities, and population genetic structures. For both species, we found a consistent lack of significant genetic variation among sampling sites across the Gulf of Carpentaria (GOC) and the Great Barrier Reef (GBR). Similarly, Bayesian clustering showed no to weak genetic partitioning across the historical Torres Strait land bridge. Both species sampled in Australia displayed population expansion signatures in tests using mtDNA and microsatellite markers. We conclude that the phylogeographic and population genetic patterns of these sea snake species do not align with the Torres Strait land bridge. This lack of population genetic structure departs from previous findings on Aipysurus sea snakes and may be linked to the association of Hydrophis species to soft sediment habitats typically found across northern Australia. These divergent patterns between the sea snake groups present the importance of considering taxon-specific attributes in formulating conservation strategies

Dispersal capacity predicts both population genetic structure and species richness in reef fishes

Dispersal is a fundamental species characteristic that should directly affect both rates of gene flow among spatially distributed populations and opportunities for speciation. Yet no single trait associated with dispersal has been demonstrated to affect both micro- and macroevolutionary patterns of diversity across a diverse biological assemblage. Here, we examine patterns of genetic differentiation and species richness in reef fishes, an assemblage of over 7,000 species comprising approximately one-third of the extant bony fishes and over one-tenth of living vertebrates. In reef fishes, dispersal occurs primarily during a planktonic larval stage. There are two major reproductive and parental investment syndromes among reef fishes, and the differences between them have implications for dispersal: (1) benthic guarding fishes lay negatively buoyant eggs, typically guarded by the male parent, and from these eggs hatch large, strongly swimming larvae; in contrast, (2) pelagic spawning fishes release small floating eggs directly into the water column, which drift unprotected before small weakly swimming larvae hatch. Using phylogenetic comparative methods, we show that benthic guarders have significantly greater population structure than pelagic spawners and additionally that taxonomic families of benthic guarders are more species rich than families of pelagic spawners. Our findings provide a compelling case for the continuity between micro- and macroevolutionary processes of biological diversification and underscore the importance of dispersalrelated traits in influencing the mode and tempo of evolution

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 onmarine 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

The Scope of Published Population Genetic Data for Indo-Pacific Marine Fauna and Future Research Opportunities in the Region

Marine biodiversity reaches its pinnacle in the tropical Indo-Pacific region, with high levels of both species richness and endemism, especially in coral reef habitats. While this pattern of biodiversity has been known to biogeographers for centuries, causal mechanisms remain enigmatic. Over the past 20 yrs, genetic markers have been employed by many researchers as a tool to elucidate patterns of biodiversity above and below the species level, as well as to make inferences about the underlying processes of diversification, demographic history, and dispersal. In a quantitative, comparative framework, these data can be synthesized to address questions about this bewildering diversity by treating species as “replicates.” However, the sheer size of the Indo-Pacific region means that the geographic and genetic scope of many species’ data sets are not complementary. Here, we describe data sets from 116 Indo-Pacific species (108 studies). With a mind to future synthetic investigations, we consider the strengths and omissions of currently published population genetic data for marine fauna of the Indo-Pacific region, as well as the geographic and taxonomic scope of the data, and suggest some ways forward for data collection and collation

Adaptive divergence in a scleractinian coral: physiological adaptation of Seriatopora hystrix to shallow and deep reef habitats

Background: Divergent natural selection across environmental gradients has been acknowledged as a major driver of population and species divergence, however its role in the diversification of scleractinian corals remains poorly understood. Recently, it was demonstrated that the brooding coral Seriatopora hystrix and its algal endosymbionts (Symbiodinium) are genetically partitioned across reef environments (0-30 m) on the far northern Great Barrier Reef. Here, we explore the potential mechanisms underlying this differentiation and assess the stability of host-symbiont associations through a reciprocal transplantation experiment across habitats ('Back Reef', 'Upper Slope' and 'Deep Slope'), in combination with molecular (mtDNA and ITS2-DGGE) and photo-physiological analyses (respirometry and HPLC)

Larval traits show temporally consistent constraints, but are decoupled from post-settlement juvenile growth, in an intertidal fish

1.Complex life-cycles may evolve to dissociate distinct developmental phases in an organism's lifetime. However, genetic or environmental factors may restrict trait independence across life stages, constraining ontogenetic trajectories. Quantifying covariance across life-stages and their temporal variability is fundamental in understanding life-history phenotypes and potential distributions and consequences for selection. 2.We studied developmental constraints in an intertidal fish (Bathygobius cocosensis: Gobiidae) with a discrete pelagic larval phase and benthic juvenile phase. We tested whether traits occurring earlier in life affected those expressed later, and whether larval traits were decoupled from post-settlement juvenile traits. Sampling distinct cohorts from three annual breeding seasons afforded tests of temporally variability in trait covariance. 3.From otoliths (fish ear stones), we measured hatch size, larval duration, pelagic growth (larval traits) and early post-settlement growth (juvenile trait) in 124 juvenile B. cocoensis. We used path analyses to model trait relationships with respect to their chronological expression, comparing models among seasons. We also modelled the effect of season and hatch date on each individual trait to quantify their inherent variability. 4.Our path analyses demonstrated a decoupling of larval traits on juvenile growth. Within the larval phase, longer larval durations resulted in greater pelagic growth, and larger size-at-settlement. There was also evidence that larger hatch size might reduce larval durations, but this effect was only marginally significant. Although pelagic and post-settlement growth were decoupled, pelagic growth had post-settlement consequences: individuals with high pelagic growth were among the largest fish at settlement, and remained among the largest early post-settlement. We observed no evidence that trait relationships varied among breeding seasons, but larval duration differed among breeding seasons, and was shorter for larvae hatching later within each season. 5.Overall, we demonstrate mixed support for the expectation that traits in different life-stages are independent. While post-settlement growth was decoupled from larval traits, pelagic development had consequences for the size of newly settled juveniles. Temporal consistency in trait covariances implies that genetic and/or environmental factors influencing them were stable over our three-year study. Our work highlights the importance of individual developmental experiences and temporal variability in understanding population distributions of life-history traits. This article is protected by copyright. All rights reserved

Genetic Divergence across Habitats in the Widespread Coral Seriatopora hystrix and Its Associated Symbiodinium

Background: Coral reefs are hotspots of biodiversity, yet processes of diversification in these ecosystems are poorly understood. The environmental heterogeneity of coral reef environments could be an important contributor to diversification, however, evidence supporting ecological speciation in corals is sparse. Here, we present data from a widespread coral species that reveals a strong association of host and symbiont lineages with specific habitats, consistent with distinct, sympatric gene pools that are maintained through ecologically-based selection.\ud \ud Methodology/Principal Findings: Populations of a common brooding coral, Seriatopora hystrix, were sampled from three adjacent reef habitats (spanning a ~30 m depth range) at three locations on the Great Barrier Reef (n = 336). The populations were assessed for genetic structure using a combination of mitochondrial (putative control region) and nuclear (three microsatellites) markers for the coral host, and the ITS2 region of the ribosomal DNA for the algal symbionts (Symbiodinium). Our results show concordant genetic partitioning of both the coral host and its symbionts across the different habitats, independent of sampling location.\ud \ud Conclusions/Significance: This study demonstrates that coral populations and their associated symbionts can be highly structured across habitats on a single reef. Coral populations from adjacent habitats were found to be genetically isolated from each other, whereas genetic similarity was maintained across similar habitat types at different locations. The most parsimonious explanation for the observed genetic partitioning across habitats is that adaptation to the local environment has caused ecological divergence of distinct genetic groups within S. hystrix

Evolving coral reef conservation with genetic information

Targeted conservation and management programs are crucial for mitigating anthropogenic threats to declining biodiversity. Although evolutionary processes underpin extant patterns of biodiversity, it is uncommon for resource managers to explicitly consider genetic data in conservation prioritization. Genetic information is inherently relevant to management because it describes genetic diversity, population connectedness, and evolutionary history; thereby typifying their behavioral traits, physiological climate tolerance, evolutionary potential, and dispersal ability. Incorporating genetic information into spatial conservation prioritization starts with reconciling the terminology and techniques used in genetics and conservation science. Genetic data vary widely in analyses and their interpretations can be challenging even for experienced geneticists. Therefore, identifying objectives, decision rules, and implementations in decision support tools specifically for management using genetic data is challenging. Here, we outline a framework for eight genetic system characteristics, their measurement, and how they could be incorporated in spatial conservation prioritization for two contrasting objectives: biodiversity preservation vs maintaining ecological function and sustainable use. We illustrate this framework with an example using data from Tridacna crocea (Lamarck, 1819) (boring giant clam) in the Coral Triangle. We find that many reefs highlighted as conservation priorities with genetic data based on genetic subregions, genetic diversity, genetic distinctness, and connectivity are not prioritized using standard practices. Moreover, different characteristics calculated from the same samples resulted in different spatial conservation priorities. Our results highlight that omitting genetic information from conservation decisions may fail to adequately represent processes regulating biodiversity, but that conservation objectives related to the choice of genetic system characteristics require careful consideration