Genetic diversity is a crucial component of biodiversity, and as such, its maintenance and preservation is of high conservation concern. Tropical environments are undergoing intense rates of environmental change, and these changes may be driving large declines in genetic diversity. However, data on genetic diversity are highly skewed towards temperate regions. The degree to which diversity loss has occurred in tropical species, particularly marine species, remains an open and important question. Here, we directly compare genomic data from modern and museum collections of two commercially harvested nearshore marine fishes ( (Equulites laterofenestra and Gazza minuta) gathered from a single location in the Philippines, spanning a century of intense environmental change. These data reveal a marked loss in genetic diversity and evidence for multiple orders of magnitude reductions in effective population size (Ne) in both species, indicating substantial genomic erosion. Such a decline highlights the long-lasting genomic consequences of anthropogenic activity and sheds light on an, until-now, invisible loss of diversity from the most biodiverse ocean region.
AbstractEvaluating the evolutionary impacts of anthropogenic activity on populations is key to understanding species resiliency and to designing effective conservation strategies. Sequencing DNA from historical specimens provides the opportunity to establish a historical baseline and empirically assess changes in genetic diversity, changes in effective population size, and selection over time. Here, we sequenced historical and contemporary samples of the cardinalfish Taeniamia zosterophora collected in 1908 and in 2021-2022 across two sites with differing human impact in the Philippines. At both sites, genetic diversity increased over time, with contemporary samples having significantly higher Watterson's θ than historical samples. This diversity increase was primarily attributable to positive selection on low-frequency alleles such that they increased toward intermediate frequencies through time. For the putatively neutral fraction of the genome, in contrast, there was a slight but significant decline in Watterson's θ at both low and high human impact sites, suggesting that drift strengthened and effective population sizes declined through time. There was more evidence for selection and greater loss of neutral diversity at the site with higher human impact. Our results provide empirical evidence for the surprising preservation of genetic diversity through the action of natural selection in the face of anthropogenic impacts.
The Smallscale Croaker, Boesemania microlepis, is a valuable fishery resource in the Mekong River basin that lacks clear biological data to understand its basic ecology and conservation management priorities. This species is common in the southernmost floodplain of the Mekong which extends from Tonlé Sap in Cambodia to the Mekong Delta in Vietnam. This floodplain is of particular biodiversity conservation concern because of the many upstream dams that restrict water flow in an ecology that relies heavily on a flood-pulse cycle. The literature regarding the biology B. microlepis in this region contains conflicting ideas that populations are both highly localized and exhibit extensive migratory behavior. We used restriction-site associated DNA to test the hypothesis that localized populations exist in the southernmost floodplain of the Mekong basin. Our data indicates high connectivity among seven sites sampled in this region supporting overall panmixia. Our results suggest a potential upstream source of propagules for this floodplain and the need for further research to clarify mechanisms driving gene flow.
Overfishing remains a threat to coral reef fishes worldwide, with large carnivores often disproportionately vulnerable. Marine protected areas (MPAs) can restore fish populations and biodiversity, but their effect has been understudied in mesophotic coral ecosystems (MCEs), particularly in the Coral Triangle. Videos were analysed from baited remote underwater video systems deployed in 2016 to investigate the assemblage structure of large carnivorous fishes at shallow (4-12 m) and mesophotic (45-96 m) depths in two of the largest and most isolated MPAs in the Philippines: an uninhabited, fully no-take MPA enacted in 1988 (Tubbataha Reefs Natural Park) and an archipelagic municipality surrounded by an extensive but not fully no-take MPA declared in 2016 (Cagayancillo). Taxa focused on were groupers (Serranidae), snappers (Lutjanidae), emperors (Lethrinidae), jacks (Carangidae) and the endangered Cheilinus undulatus (Labridae). Mean abundance and species richness were not greater in TRNP than in Cagayancillo regardless of depth despite long-term protection in the former. Limited impacts of fishing in Cagayancillo may explain this result. Differentiation of fish assemblages was evident between TRNP and Cagayancillo but more obvious between depths at each location, probably due more to habitat than MPA effects. In Cagayancillo, overall carnivorous reef fish, grouper and jack mean abundance were 2, 2 and 10 times higher, respectively, at mesophotic depths, suggesting that MCEs can serve as deep refugia from fishing. These findings of differentiation between depths and higher abundance of certain taxa in mesophotic depths emphasize that MCEs are distinct from shallow reefs, serve as important habitat for species susceptible to overfishing and, thus, must be explicitly included in the design of MPAs. This study also highlights the value of maintaining strict protection of MPAs like TRNP for the Coral Triangle and an opportunity to safeguard intact fish assemblages in Cagayancillo by expanding its no-take zones.
The eastern oyster, Crassostrea virginica, is divided into four populations along the western North Atlantic, however, the only published mitochondrial genome sequence was assembled using one individual in Delaware. This study aimed to (1) assemble C. virginica mitochondrial genomes from Texas with pooled restriction-site-associated DNA sequencing (ezRAD), (2) evaluate the validity of the mitochondrial genome assemblies including comparison with Sanger sequencing data, and (3) evaluate genetic differentiation both between the Delaware and Texas genomes, as well as among three bays in Texas. The pooled-genome-assembled-genomes (PAGs) from Texas exhibited several characteristics indicating that they were valid, including elevated nucleotide diversity in non-coding and the third position of codons, placement as the sister haplotype of the genome from Delaware in a phylogenetic reconstruction of Crassostrea mitochondrial genomes, and a lack of genetic structure in the ND4 gene among the three Texas bays as was found with Sanger amplicons in samples from the same bays several years prior. In the comparison between the Delaware and Texas genome, 27 of 38 coding regions exhibited variability between the two populations, which were differentiated by 273 mutations, versus 1–13 mutations among the Texas samples. Using the full PAGs, there was no additional evidence for population structure among the three Texas bays. While population genetics is rapidly moving towards larger high-density datasets, studies of mitochondrial DNA (and genomes) can be particularly useful for comparing historic data prior to the modern era of genomics. As such, being able to reliably compile mitochondrial genomes from genomic data can improve the ability to compare results across studies.
Aim: Humans are unintentionally affecting the evolution of fishery species directly through exploitation and indirectly by altering climate. We aim to test for a relationship between biogeographic patterns in the shell phenotypes of an over-exploited shellfish and the presence of humans to identify human-mediated adaptive trade-offs. The implications of these trade-offs are discussed with respect to the sustainability of the fishery. Taxon: The endemic Hawaiian intertidal limpet, 'opihi makaiauli (Patellagastropoda, Nacellidae, Cellana exarata) Methods: We surveyed phenotypic characters associated with temperature and predation avoidance across the entire species range and tested for differences in the relationship between these characters and latitude, on islands with and without humans. Results: Among all limpets surveyed, there was a bimodal distribution in shell colour (light, dark) and a parapatric pattern of shell coloration across the archipelago with lighter shells being prevalent on the uninhabited islands and darker, more camouflaged shells being prevalent on the inhabited islands. On the cooler, uninhabited islands, all morphometric characters associated with thermal avoidance (surface area, height and doming) increased with decreasing latitude. On the hotter, inhabited islands, however, shells were flatter, less variable and less adapted for avoiding thermal stress than predation. Main Conclusions: The biogeographic patterns in shell phenotype and previous genetic studies suggest that the population is beginning to bifurcate in response to disruptive and directional selection as well as geographic isolation between the islands with and without humans. Decreased phenotypic and genetic diversity on the inhabited islands despite much larger populations of 'opihi suggests a prominent historical bottleneck. The prevalence of maladaptive dark, flat phenotypes for thermal avoidance on the inhabited islands suggests that predation is a stronger selective force, driving adaptive trade-offs in shape and colour. We propose that this is likely a case of fisheries-induced evolution and a millennium of harvesting is the most likely selective pressure driving the observed biogeographic patterns in shell morphology. The flatter, darker shells will allow body temperatures to rise higher in direct sunlight, therefore we hypothesize that the thermal niche of 'opihi is narrower on inhabited islands and will continue to narrow as Earth warms.
Impacts of urban development on aquatic populations are often complex and difficult to ascertain, but population genetic analysis has allowed researchers to monitor and estimate gene flow in the context of existing and future hydroelectric projects. The Lower Mekong Basin is undergoing rapid hydroelectric development with around 50 completed and under-construction dams and 95 planned dams. The authors investigated the baseline genetic diversity of two exploited migratory fishes, the mud carpHenicorhynchus lobatus(five locations), and the rat-faced pangasiid catfish,Helicophagus leptorhynchus(two locations), in the Lower Mekong Basin using the genomic double digest restriction site-associated DNA (ddRAD) sequencing method. In both species, fish sampled upstream of Khone Falls were differentiated from those collected at other sites, andN(e)estimates at the site above the falls were lower than those at other sites. This was the first study to utilize thousands of RAD-generated single nucleotide polymorphisms to indicate that the Mekong's Khone Falls are a potential barrier to gene flow for these two moderately migratory species. The recent completion of the Don Sahong dam across one of the only channels for migratory fishes through Khone Falls may further exacerbate signatures of isolation and continue to disrupt the migration patterns of regionally vital food fishes. In addition,H. lobatuspopulations downstream of Khone Falls, including the 3S Basin and Tonle Sap system, displayed robust connectivity. Potential obstruction of migration pathways between these river systems resulting from future dam construction may limit dispersal, which has led to elevated inbreeding rates and even local extirpation in other fragmented riverine species.
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 phi(ST), and these phi(ST) 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 phi(ST) 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 phi(ST) that was very similar to empirical distributions observed across five putative barriers to gene flow. Three of these barriers had median phi(ST) 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 phi(ST), 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 phi(ST )values that range from 0 to nearly 0.5.
An understanding of the genetic composition of populations across management boundaries is vital to developing successful strategies for sustaining biodiversity and food resources. This is especially important in ecosystems where habitat fragmentation has altered baseline patterns of gene flow, dividing natural populations into smaller subpopulations and increasing potential loss of genetic variation through genetic drift. River systems can be highly fragmented by dams built for flow regulation and hydropower. We used reduced-representation sequencing to examine genomic patterns in an exploited catfish, Hemibagrus spilopterus, in a hotspot of biodiversity and hydropower development-the Mekong River basin. Our results revealed the presence of 2 highly divergent coexisting genetic lineages which may be cryptic species. Within the lineage with the greatest sample sizes, pairwise F-ST values, principal component analysis, and a STRUCTURE analysis all suggest that long-distance migration is not common across the Lower Mekong Basin, even in areas where flood-pulse hydrology has limited genetic divergence. In tributaries, effective population size estimates were at least an order of magnitude lower than in the Mekong mainstream indicating these populations may be more vulnerable to perturbations such as human-induced fragmentation. Fish isolated upstream of several dams in one tributary exhibited particularly low genetic diversity, high amounts of relatedness, and a level of inbreeding (G(IS) = 0.51) that has been associated with inbreeding depression in other outcrossing species. Our results highlight the importance of assessing genetic structure and diversity in riverine fisheries populations across proposed dam development sites for the preservation of these critically important resources.
Aim Mayr's central-peripheral population model (CCPM) describes the marked differences between central and peripheral populations in genetic diversity, gene flow, and census size. When isolation leads to genetic divergence, these peripheral populations have high evolutionary value and can influence biogeographic patterns. In tropical marine species with pelagic larvae, powerful western-boundary currents have great potential to shape the genetic characteristics of peripheral populations at latitudinal extremes. We tested for the genetic patterns expected by the CCPM in peripheral populations that are located within the Kuroshio Current for the Indo-Pacific reef fish, Caesio cuning. Methods We used a panel of 2,677 SNPs generated from restriction site-associated DNA (RAD) sequencing to investigate genetic diversity, relatedness, effective population size, and spatial patterns of population connectivity from central to peripheral populations of C. cuning along the Kuroshio Current. Results Principal component and cluster analyses indicated a genetically distinct lineage at the periphery of the C. cuning species range and examination of SNPs putatively under divergent selection suggested potential for local adaptation in this region. We found signatures of isolation-by-distance and significant genetic differences between nearly all sites. Sites closest to the periphery exhibited increased within-population relatedness and decreased effective population size. Main Conclusions Despite the potential for homogenizing gene flow along the Kuroshio Current, peripheral populations in C. cuning conform to the predictions of the CCPM. While oceanography, habitat availability, and dispersal ability are all likely to shape the patterns found in C. cuning across this central-peripheral junction, the impacts of genetic drift and natural selection in increasing smaller peripheral populations appear to be probable influences on the lineage divergence found in the Ryukyu Islands.
Inducing defenses to deter predators is a necessary process theorized to incur costs. Although studies have investigated defense trade-offs, quantifying trade-offs is challenging and costs are often inferred. Additionally, prey employ strategies to reduce costs, making costs difficult to predict. Our purpose was to investigate induced defense costs by characterizing the defense mechanisms and costs in eastern oysters (Crassostrea virginica). In the field, newly-settled oysters exposed to blue crab (Callinectes sapidus) exudates grew stronger shells containing less percent organic material than oysters in controls. In natural populations, shell density was negatively correlated with shell thickness, further suggesting oysters thicken their shells by increasing low-density calcium carbonate. Reproductive investment showed an increasingly negative relationship with thickness as density decreased (and induction increased). In a laboratory experiment, oysters exposed to a temporal gradient in risk grew heavier shells in all crab treatments, but only grew stronger shells under constant exposure. Collectively, these results suggest oysters initially react to predators by adding inexpensive calcium carbonate to their shells to quickly outgrow risk. However, in high-risk environments, oysters may increase the production of costly organic material to increase the shell strength. Thus, oysters demonstrate a two-tier mechanism allowing them to cheaply escape predation at lower risk but to build stronger shells at greater expense when warranted. These results illuminate the complex strategies prey deploy to balance predation risk and defense costs as well as the importance of understanding these strategies to accurately predict predator effects.
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. It contributes to the informatics stack – Biocode Commons – of the Genomic Observatories Network (https://gigascience.biomedcentral.com/articles/10.1186/2047-217X-3-2). The GeOMe project interface enables administrators to plan and execute field based sample collection efforts. GeOMe projects specify a core set of sample metadata fields based on community standard vocabularies and also includes plugins for associating samples with photos, subsamples, NextGen sequence metadata, and permits. Users can upload their own expedition-specific metadata, which contributes to the overall project dataset while providing the user a convenient method for updating and refining their contributed data. GeOMe provides connection points to the Global Biodiversity Information Facility and archived genetic data stored in the National Center for Biotechnology Information's (NCBI's) Sequence Read Archive (SRA), linking specimens and seqeuences via unique persistent identifiers.
The Marianas Trench Marine National Monument (MNM) currently extends policy-based protection to deep-sea ecosystems contained within it, but managers require better understanding of the current knowledge and knowledge gaps about these ecosystems to guide decision-making. To address this need, we present a case study of the Marianas Trench MNM using in-depth interviews to determine scientists’ (1) current understanding of anthropogenic drivers of change and system vulnerability in deep-sea ecosystems; and (2) perceptions of the least understood deep-sea ecosystems and processes in the Marianas Trench MNM, and which of these, if any, should be research priorities to fill knowledge gaps about these systems and the impacts from anthropogenic drivers of change. Interview respondents shared similar views on the current knowledge of deep-sea ecosystems and potential anthropogenic drivers of change in the Marianas Trench MNM. Respondents also identified trench and deep pelagic (bathyal, abyssal, and hadal zones) ecosystems as the least understood, and highlighted climate change, litter and waste, mining and fishing, and interactions between these drivers of change as critical knowledge gaps. To fill key knowledge gaps and inform conservation decision-making, respondents identified the need for monitoring networks and time-series data. Our approach demonstrates how in-depth interviews can be used to elicit knowledge to inform decision-making in data-limited situations.
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.
The invasion of the western Atlantic Ocean by the Indo-Pacific red lionfish (Pterois volitans) has had devastating consequences for marine ecosystems. Estimating the number of colonizing lionfish can be useful in identifying the introduction pathway and can inform policy decisions aimed at preventing similar invasions. It is well-established that at least ten lionfish were initially introduced. However, that estimate has not faced probabilistic scrutiny and is based solely on the number of haplotypes in the maternally-inherited mitochondrial control region. To rigorously estimate the number of lionfish that were introduced, we used a forward-time, Wright-Fisher, population genetic model in concert with a demographic, life-history model to simulate the invasion across a range of source population sizes and colonizing population fecundities. Assuming a balanced sex ratio and no Allee effects, the simulations indicate that the Atlantic population was founded by 118 (54–514, 95% HPD) lionfish from the Indo-Pacific, the Caribbean by 84 (22–328, 95% HPD) lionfish from the Atlantic, and the Gulf of Mexico by at least 114 (no upper bound on 95% HPD) lionfish from the Caribbean. Increasing the size, and therefore diversity, of the Indo-Pacific source population and fecundity of the founding population caused the number of colonists to decrease, but with rapidly diminishing returns. When the simulation was parameterized to minimize the number of colonists (high θ and relative fecundity), 96 (48–216, 95% HPD) colonists were most likely. In a more realistic scenario with Allee effects (e.g., 50% reduction in fecundity) plaguing the colonists, the most likely number of lionfish increased to 272 (106–950, 95% HPD). These results, in combination with other published data, support the hypothesis that lionfish were introduced to the Atlantic via the aquarium trade, rather than shipping. When building the model employed here, we made assumptions that minimize the number of colonists, such as the lionfish being introduced in a single event. While we conservatively modelled the introduction pathway as a single release of lionfish in one location, it is more likely that a combination of smaller and larger releases from a variety of aquarium trade stakeholders occurred near Miami, Florida, which could have led to even larger numbers of colonists than simulated here. Efforts to prevent future invasions via the aquarium trade should focus on the education of stakeholders and the prohibition of release, with adequate rewards for compliance and penalties for violations.
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. It contributes to the informatics stack – Biocode Commons – of the Genomic Observatories Network (https://gigascience.biomedcentral.com/articles/10.1186/2047-217X-3-2). While public databases have served as vital repositories for nucleotide sequences, they do not accession all the metadata required for ecological or evolutionary analyses. These metadata are especially important for process oriented, time-series research, as for example, at Long Term Ecological Research (LTER) sites or longitudinal public health studies. 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 standards-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 publically archived genetic sequence data in a structured manner, GeOMe provides an important linchpin across all levels of biodiversity.
The invasion of the western Atlantic Ocean by the Indo-Pacific red lionfish (Pterois volitans) has had devastating consequences for marine ecosystems. Estimating the number of colonizing lionfish can be useful in identifying the introduction pathway and can inform policy decisions aimed at preventing similar invasions. It is well-established that at least ten lionfish were initially introduced. However, that estimate has not faced statistical scrutiny and is based solely on the number of haplotypes in the maternally-inherited mitochondrial control region observed in samples from the western Atlantic Ocean. To rigorously estimate the number of lionfish introduced, we used a forward-time, Wright-Fisher, population genetic model of the mitochondrial control region in concert with a demographic life-history model to simulate the invasion. The colonization of the western North Atlantic and subsequent spread to the Caribbean and Gulf of Mexico were modeled as single introductions of 1-800 females, which should conservatively estimate the most likely number of colonizing lionfish relative to a model with multiple introductions. Assuming a balanced sex ratio and no Allee effects, the simulations indicate that the Atlantic population was most likely founded by 118 (54-514, 95% HPD) lionfish from the Indo-Pacific, the Caribbean by 84 (22-328, 95% HPD) lionfish from the Atlantic, and the Gulf of Mexico by at least 114 (no upper bound on 95% HPD) lionfish from the Caribbean. Considering the additional possibilities that (1) multiple Indo-Pacific populations colonized the Atlantic and (2) Allee effects (e.g. 50% reduction in fecundity) plagued the colonists, the most likely number of lionfish increased to 180 (88-416, 95% HPD). These results, in combination with all other published data, support the hypothesis that lionfish were introduced to the Atlantic via the aquarium trade, rather than shipping. The most parsimonious introduction pathway is a single release of lionfish in one location, but it seems likely that a combination of smaller and larger releases from a variety of aquarium trade stakeholders occurred near Miami, Florida. Efforts to prevent future invasions via the aquarium trade should focus on the education of stakeholders and the prohibition of release, with adequate rewards for compliance and penalties for violations.
Indo-Pacific lionfish (Pterois volitans and P. miles) recently invaded Western Atlantic waters, rapidly spreading through the Caribbean and Gulf of Mexico (GoM). Previous genetic analyses using the mitochondrial d-loop determined that populations in the Western North Atlantic (NA) region have up to nine haplotypes, whereas Caribbean populations contain four of the North Atlantic haplotypes. The genetic composition of GoM populations, reported here for the first time, could lend insight into the pathway of dispersal into the GoM and better understanding of the biogeography of this recent invader. Here, we determined the genetic composition of lionfish throughout the GoM and compared haplotype composition to Caribbean and North Atlantic regions. We found that GoM samples contained only three d-loop haplotypes that are common in the Caribbean and North Atlantic. The genetic structure differed significantly among the three regions (AMOVA:Φ CT = 0.062; p = 0.001), but we found no differences between locations within regions (AMOVA:Φ SC = 0.005; p = 0.092). The composition of GoM samples most closely matches the composition of Caribbean samples indicating that Caribbean populations are the likely source of the GoM populations. As each region was successively invaded, a drop in haplotype diversity and changes in haplotype frequencies occurred indicating dispersal limitation across basin boundaries and founder effects within each basin. The lack of differentiation within regions indicates rapid population growth and unfettered dispersal within basins after initial colonization. We find no evidence of secondary invasions within samples. With well-established populations, the probability of detecting a secondary invasion is minuscule.