ABSTRACT
In the present study, first generation DNA sequencing (mitochondrial cytochrome c oxidase subunit one, COI) and reduced-representative genomic RADseq data were used to understand the patterns and processes of diversification of the velvet worm, Peripatopsis sedgwicki species complex across its distribution range in South Africa. For the RADseq data, three datasets (two primary and one supplementary) were generated corresponding to 1,259-11,468 SNPs, in order to assess the diversity and phylogeography of the species complex. Tree topologies for the two primary datasets were inferred using maximum likelihood and Bayesian inferences methods. Phylogenetic analyses using the COI datasets retrieved four distinct, well-supported clades within the species complex. Five species delimitation methods applied to the COI data (ASAP, bPTP, bGMYC, STACEY and iBPP) all showed support for the distinction of the Fort Fordyce Nature Reserve specimens. In the main P. sedgwicki species complex, the species delimitation methods revealed a variable number of operational taxonomic units and overestimated the number of putative taxa. Divergence time estimates coupled with the geographic exclusivity of species and phylogeographic results suggest recent cladogenesis during the Plio/Pleistocene. The RADseq data were subjected to a principal components analysis and a discriminant analysis of principal components, under a maximum-likelihood framework. The latter results corroborate the four main clades observed using the COI data, however, applying additional filtering revealed additional diversity. The high overall congruence observed between the RADseq data and COI data suggest that first generation sequence data remain a cheap and effective method for evolutionary studies, although RADseq does provide a far greater resolution of contemporary temporo-spatial patterns.
Subject(s)
Phylogeny , Animals , Phylogeography , Sequence Analysis, DNA , Bayes Theorem , South Africa , Electron Transport Complex IV/geneticsABSTRACT
Genomic information can aid in the establishment of sustainable management plans for commercially exploited marine fishes, aiding in the long-term conservation of these resources. The southern African hakes (Merluccius capensis and M. paradoxus) are commercially valuable demersal fishes with similar distribution ranges but exhibiting contrasting life histories. Using a comparative framework based on Pool-Seq genome-wide SNP data, we investigated whether the evolutionary processes that shaped extant patterns of diversity and divergence are shared among these two congeneric fishes, or unique to each one. Our findings revealed that M. capensis and M. paradoxus show similar levels of genome-wide diversity, despite different census sizes and life-history features. In addition, M. capensis shows three highly structured geographic populations across the Benguela Current region (one in the northern Benguela and two in the southern Benguela), with no consistent genome-environment associations detected. In contrast, although population structure and outlier analyses suggested panmixia for M. paradoxus, reconstruction of its demographic history suggested the presence of an Atlantic-Indian Ocean subtle substructuring pattern. Therefore, it appears that M. paradoxus might be composed by two highly connected populations, one in the Atlantic and one in the southwest Indian Ocean. The reported similar low levels of genomic diversity, as well as newly discovered genetically distinct populations in both hake species can thus assist in informing and improving conservation and management plans for the commercially important southern African Merluccius.
ABSTRACT
Anthropogenic-induced climate change is having profound impacts on aquatic ecosystems, and the resilience of fish populations will be determined by their response to these impacts. The northern Namibian coast is an ocean warming hotspot, with temperatures rising faster than the global average. The rapid warming in Namibia has had considerable impacts on marine fauna, such as the southern extension of the distribution of Argyrosomus coronus from southern Angola into northern Namibian waters, where it now overlaps and hybridizes with the closely related Namibian species, A. inodorus. Understanding how these species (and their hybrids) perform at current and future temperatures is vital to optimize adaptive management for Argyrosomus species. Intermittent flow-through respirometry was used to quantify standard and maximum metabolic rates for Argyrosomus individuals across a range of temperatures. The modelled aerobic scope (AS) of A. inodorus was notably higher at cooler temperatures (12, 15, 18 and 21°C) compared with that of A. coronus, whereas the AS was similar at 24°C. Although only five hybrids were detected and three modelled, their AS was in the upper bounds of the models at 15, 18 and 24°C. These findings suggest that the warming conditions in northern Namibia may increasingly favour A. coronus and promote the poleward movement of the leading edge of their southern distribution. In contrast, the poor aerobic performance of both species at cold temperatures (12°C) suggests that the cold water associated with the permanent Lüderitz Upwelling Cell in the south may constrain both species to central Namibia. This is most concerning for A. inodorus because it may be subjected to a considerable coastal squeeze.
ABSTRACT
Integrative and proactive conservation approaches are critical to the long-term persistence of biodiversity. Molecular data can provide important information on evolutionary processes necessary for conserving multiple levels of biodiversity (genes, populations, species, and ecosystems). However, molecular data are rarely used to guide spatial conservation decision-making. Here, we bridge the fields of molecular ecology (ME) and systematic conservation planning (SCP) (the 'why') to build a foundation for the inclusion of molecular data into spatial conservation planning tools (the 'how'), and provide a practical guide for implementing this integrative approach for both conservation planners and molecular ecologists. The proposed framework enhances interdisciplinary capacity, which is crucial to achieving the ambitious global conservation goals envisioned for the next decade.
Subject(s)
Conservation of Natural Resources , Ecosystem , Ecology , Biodiversity , Biological EvolutionABSTRACT
Over the last century, many shark populations have declined, primarily due to overexploitation in commercial, artisanal and recreational fisheries. In addition, in some locations the use of shark control programs also has had an impact on shark numbers. Still, there is a general perception that populations of large ocean predators cover wide areas and therefore their diversity is less susceptible to local anthropogenic disturbance. Here we report on temporal genomic analyses of tiger shark (Galeocerdo cuvier) DNA samples that were collected from eastern Australia over the past century. Using Single Nucleotide Polymorphism (SNP) loci, we documented a significant change in genetic composition of tiger sharks born between ~1939 and 2015. The change was most likely due to a shift over time in the relative contribution of two well-differentiated, but hitherto cryptic populations. Our data strongly indicate a dramatic shift in the relative contribution of these two populations to the overall tiger shark abundance on the east coast of Australia, possibly associated with differences in direct or indirect exploitation rates.
Subject(s)
Sharks , Animals , Australia , Fisheries , Genomics , Retrospective Studies , Sharks/geneticsABSTRACT
Targeted sequencing is an increasingly popular next-generation sequencing (NGS) approach for studying populations that involves focusing sequencing efforts on specific parts of the genome of a species of interest. Methodologies and tools for designing targeted baits are scarce but in high demand. Here, we present specific guidelines and considerations for designing capture sequencing experiments for population genetics for both neutral genomic regions and regions subject to selection. We describe the bait design process for three diverse fish species: Atlantic salmon, Atlantic cod and tiger shark, which was carried out in our research group, and provide an evaluation of the performance of our approach across both historical and modern samples. The workflow used for designing these three bait sets has been implemented in the R-package supeRbaits, which encompasses our considerations and guidelines for bait design for the benefit of researchers and practitioners. The supeRbaits R-package is user-friendly and versatile. It is written in C++ and implemented in R. supeRbaits and its manual are available from Github: https://github.com/BelenJM/supeRbaits.
Subject(s)
High-Throughput Nucleotide Sequencing , Animals , DNA/genetics , Genetics, Population , Genomics/methods , High-Throughput Nucleotide Sequencing/methods , Sequence Analysis, DNA/methods , FishesABSTRACT
Characterising and predicting species responses to anthropogenic global change is one of the key challenges in contemporary ecology and conservation. The sensitivity of marine species to climate change is increasingly being described with forecasted species distributions, yet these rarely account for population level processes such as genomic variation and local adaptation. This study compares inter- and intraspecific patterns of biological composition to determine how vulnerability to climate change, and its environmental drivers, vary across species and populations. We compare species trajectories for three ecologically important southern African marine invertebrates at two time points in the future, both at the species level, with correlative species distribution models, and at the population level, with gradient forest models. Reported range shifts are species-specific and include both predicted range gains and losses. Forecasted species responses to climate change are strongly influenced by changes in a suite of environmental variables, from sea surface salinity and sea surface temperature, to minimum air temperature. Our results further suggest a mismatch between future habitat suitability (where species can remain in their ecological niche) and genomic vulnerability (where populations retain their genomic composition), highlighting the inter- and intraspecific variability in species' sensitivity to global change. Overall, this study demonstrates the importance of considering species and population level climatic vulnerability when proactively managing coastal marine ecosystems in the Anthropocene.
Subject(s)
Climate Change , Ecosystem , Forests , Genomics , TemperatureABSTRACT
BACKGROUND: As global change and anthropogenic pressures continue to increase, conservation and management increasingly needs to consider species' potential to adapt to novel environmental conditions. Therefore, it is imperative to characterise the main selective forces acting on ecosystems, and how these may influence the evolutionary potential of populations and species. Using a multi-model seascape genomics approach, we compare putative environmental drivers of selection in three sympatric southern African marine invertebrates with contrasting ecology and life histories: Cape urchin (Parechinus angulosus), Common shore crab (Cyclograpsus punctatus), and Granular limpet (Scutellastra granularis). RESULTS: Using pooled (Pool-seq), restriction-site associated DNA sequencing (RAD-seq), and seven outlier detection methods, we characterise genomic variation between populations along a strong biogeographical gradient. Of the three species, only S. granularis showed significant isolation-by-distance, and isolation-by-environment driven by sea surface temperatures (SST). In contrast, sea surface salinity (SSS) and range in air temperature correlated more strongly with genomic variation in C. punctatus and P. angulosus. Differences were also found in genomic structuring between the three species, with outlier loci contributing to two clusters in the East and West Coasts for S. granularis and P. angulosus, but not for C. punctatus. CONCLUSION: The findings illustrate distinct evolutionary potential across species, suggesting that species-specific habitat requirements and responses to environmental stresses may be better predictors of evolutionary patterns than the strong environmental gradients within the region. We also found large discrepancies between outlier detection methodologies, and thus offer a novel multi-model approach to identifying the principal environmental selection forces acting on species. Overall, this work highlights how adding a comparative approach to seascape genomics (both with multiple models and species) can elucidate the intricate evolutionary responses of ecosystems to global change.
Subject(s)
Brachyura/genetics , Ecosystem , Gastropoda/genetics , Genetics, Population , Sea Urchins/genetics , Selection, Genetic , Animals , Genomics , Polymorphism, Single Nucleotide , Sequence Analysis, DNA , TemperatureABSTRACT
Understanding the demographic history of introduced populations is essential for unravelling their invasive potential and adaptability to a novel environment. To this end, levels of genetic diversity within the native and invasive range of a species are often compared. Most studies, however, focus solely on contemporary samples, relying heavily on the premise that the historic population structure within the native range has been maintained over time. Here, we assess this assumption by conducting a three-way comparison of the genetic diversity of native (historic and contemporary) and invasive (contemporary) smallmouth bass (Micropterus dolomieu) populations. Analyses of a total of 572 M. dolomieu samples, representing the contemporary invasive South African range, contemporary and historical native USA range (dating back to the 1930s when these fish were first introduced into South Africa), revealed that the historical native range had higher genetic diversity levels when compared to both contemporary native and invasive ranges. These results suggest that both contemporary populations experienced a recent genetic bottleneck. Furthermore, the invasive range displayed significant population structure, whereas both historical and contemporary native US populations revealed higher levels of admixture. Comparison of contemporary and historical samples showed both a historic introduction of M. dolomieu and a more recent introduction, thereby demonstrating that undocumented introductions of this species have occurred. Although multiple introductions might have contributed to the high levels of genetic diversity in the invaded range, we discuss alternative factors that may have been responsible for the elevated levels of genetic diversity and highlight the importance of incorporating historic specimens into demographic analyses.
ABSTRACT
Introgressive hybridization between Micropterus dolomieu and Micropterus salmoides was assessed in their invaded South African range using nine microsatellite markers and two mtDNA gene regions. Although M. dolomieu and M. salmoides are distantly related, indicated by the large uncorrected pairwise distances observed between the two species, mitochondrial introgression and unidirectional admixture was detected.
Subject(s)
Bass/genetics , Hybridization, Genetic , Introduced Species , Animals , DNA, Mitochondrial/genetics , Microsatellite RepeatsABSTRACT
Gallet et al. (2018) studied the effect of two selection regimes on the maintenance of polymorphism in experimental populations. They took two strains of Escherichia coli, each resistant to a different antibiotic, evolved them in culture conditions representing "soft" or "hard" selective regimes, and measured polymorphism levels for three to five transfers. Their results supported theoretical predictions that only "soft" selection maintains polymorphism, highlighting the importance of experimental studies to understand maintenance of variation in nature.
ABSTRACT
BACKGROUND: Genomic tools are increasingly being used on non-model organisms to provide insights into population structure and variability, including signals of selection. However, most studies are carried out in regions with distinct environmental gradients or across large geographical areas, in which local adaptation is expected to occur. Therefore, the focus of this study is to characterize genomic variation and selective signals over short geographic areas within a largely homogeneous region. To assess adaptive signals between microhabitats within the rocky shore, we compared genomic variation between the Cape urchin (Parechinus angulosus), which is a low to mid-shore species, and the Granular limpet (Scutellastra granularis), a high shore specialist. RESULTS: Using pooled restriction site associated DNA (RAD) sequencing, we described patterns of genomic variation and identified outlier loci in both species. We found relatively low numbers of outlier SNPs within each species, and identified outlier genes associated with different selective pressures than those previously identified in studies conducted over larger environmental gradients. The number of population-specific outlier loci differed between species, likely owing to differential selective pressures within the intertidal environment. Interestingly, the outlier loci were highly differentiated within the two northernmost populations for both species, suggesting that unique evolutionary forces are acting on marine invertebrates within this region. CONCLUSIONS: Our study provides a background for comparative genomic studies focused on non-model species, as well as a baseline for the adaptive potential of marine invertebrates along the South African west coast. We also discuss the caveats associated with Pool-seq and potential biases of sequencing coverage on downstream genomic metrics. The findings provide evidence of species-specific selective pressures within a homogeneous environment, and suggest that selective forces acting on small scales are just as crucial to acknowledge as those acting on larger scales. As a whole, our findings imply that future population genomic studies should expand from focusing on model organisms and/or studying heterogeneous regions to better understand the evolutionary processes shaping current and future biodiversity patterns, particularly when used in a comparative phylogeographic context.
Subject(s)
Biological Evolution , Gastropoda/genetics , Genetic Variation , Genetics, Population , Sea Urchins/genetics , Animals , Phylogeography , Species SpecificityABSTRACT
Growing threats to biodiversity and global alteration of habitats and species distributions make it increasingly necessary to consider evolutionary patterns in conservation decision making. Yet, there is no clear-cut guidance on how genetic features can be incorporated into conservation-planning processes, despite multiple molecular markers and several genetic metrics for each marker type to choose from. Genetic patterns differ between species, but the potential tradeoffs among genetic objectives for multiple species in conservation planning are currently understudied. We compared spatial conservation prioritizations derived from 2 metrics of genetic diversity (nucleotide and haplotype diversity) and 2 metrics of genetic isolation (private haplotypes and local genetic differentiation) in mitochondrial DNA of 5 marine species. We compared outcomes of conservation plans based only on habitat representation with plans based on genetic data and habitat representation. Fewer priority areas were selected for conservation plans based solely on habitat representation than on plans that included habitat and genetic data. All 4 genetic metrics selected approximately similar conservation-priority areas, which is likely a result of prioritizing genetic patterns across a genetically diverse array of species. Largely, our results suggest that multispecies genetic conservation objectives are vital to creating protected-area networks that appropriately preserve community-level evolutionary patterns.
Subject(s)
Biodiversity , Conservation of Natural Resources , Reproductive Isolation , Biological Evolution , EcosystemABSTRACT
Environmental gradients have been shown to disrupt gene flow in marine species, yet their influence in structuring populations at depth remains poorly understood. The Cape hakes (Merluccius paradoxus and M. capensis) are demersal species co-occurring in the Benguela Current system, where decades of intense fishing resulted in severely depleted stocks in the past. Previous studies identified conflicting mtDNA genetic substructuring patterns and thus contrasting evolutionary trajectories for both species. Using 10 microsatellite loci, the control region of mtDNA and employing a seascape genetics approach, we investigated genetic connectivity and the impact of prolonged exploitation in the two species, which are characterized by different patterns of fishing pressure. Three consecutive years were sampled covering the entire distribution (N = 2100 fishes). Despite large estimated population sizes, both species exhibited low levels of contemporary genetic diversity (0.581 < HE < 0.692), implying that fishing has had a significant impact on their genetic composition and evolutionary trajectories. Further, for M. paradoxus, significant temporal, but not spatial, divergence points to the presence of genetic chaotic patchiness. In contrast, M. capensis exhibited a clear latitudinal cline in genetic differentiation between Namibia and South Africa (FST = 0.063, P < 0.05), with low (0.2% per generation) estimates of contemporary gene flow. Seascape analyses reveal an association with bathymetry and upwelling events, suggesting that adaptation to local environmental conditions may drive genetic differentiation in M. capensis. Importantly, our results highlight the need for temporal sampling in disentangling the complex factors that impact population divergence in marine fishes.
Subject(s)
Fisheries , Gadiformes/genetics , Genetic Variation , Genetics, Population , Animals , DNA, Mitochondrial/genetics , Gene Flow , Microsatellite Repeats , Namibia , South Africa , Spatio-Temporal AnalysisABSTRACT
In the marine environment, an increasing number of studies have documented introgression and hybridization using genetic markers. Hybridization appears to occur preferentially between sister-species, with the probability of introgression decreasing with an increase in evolutionary divergence. Exceptions to this pattern were reported for the Cape hakes (Merluccius capensis and M. paradoxus), two distantly related Merluciidae species that diverged 3-4.2 million years ago. Yet, it is expected that contemporary hybridization between such divergent species would result in reduced hybrid fitness. We analysed 1,137 hake individuals using nine microsatellite markers and control region mtDNA data to assess the validity of the described hybridization event. To distinguish between interbreeding, ancestral polymorphism and homplasy we sequenced the flanking region of the most divergent microsatellite marker. Simulation and empirical analyses showed that hybrid identification significantly varied with the number of markers, model and approach used. Phylogenetic analyses based on the sequences of the flanking region of Mmerhk-3b, combined with the absence of mito-nuclear discordance, suggest that previously reported hybridization between M. paradoxus and M. capensis cannot be substantiated. Our findings highlight the need to conduct a priori simulation studies to establish the suitability of a particular set of microsatellite loci for detecting multiple hybridization events. In our example, the identification of hybrids was severely influenced by the number of loci and their variability, as well as the different models employed. More importantly, we provide quantifiable evidence showing that homoplasy mimics the effects of heterospecific crossings which can lead to the incorrect identification of hybridization.
ABSTRACT
Despite increasing awareness of large-scale climate-driven distribution shifts in the marine environment, no study has linked rapid ocean warming to a shift in distribution and consequent hybridization of a marine fish species. This study describes rapid warming (0.8 °C per decade) in the coastal waters of the Angola-Benguela Frontal Zone over the last three decades and a concomitant shift by a temperature sensitive coastal fish species (Argyrosomus coronus) southward from Angola into Namibia. In this context, rapid shifts in distribution across Economic Exclusive Zones will complicate the management of fishes, particularly when there is a lack of congruence in the fisheries policy between nations. Evidence for recent hybridization between A. coronus and a congener, A. inodorus, indicate that the rapid shift in distribution of A. coronus has placed adults of the two species in contact during their spawning events. Ocean warming may therefore revert established species isolation mechanisms and alter the evolutionary history of fishes. While the consequences of the hybridization on the production of the resource remain unclear, this will most likely introduce additional layers of complexity to their management.
Subject(s)
Animal Distribution/physiology , Conservation of Natural Resources/methods , Global Warming/statistics & numerical data , Hybridization, Genetic/physiology , Perciformes/genetics , Seawater/chemistry , Angola , Animals , Atlantic Ocean , Fisheries/legislation & jurisprudence , Fisheries/methods , Fisheries/statistics & numerical data , Namibia , Perciformes/physiology , TemperatureABSTRACT
Contemporary patterns of genetic diversity and population connectivity within species can be influenced by both historical and contemporary barriers to gene flow. In the marine environment, present day oceanographic features such as currents, fronts and upwelling systems can influence dispersal of eggs/larvae and/juveniles/adults, shaping population substructuring. The Benguela Current system in the southeastern Atlantic is one of the oldest upwelling systems in the world, and provides a unique opportunity to investigate the relative influence of contemporary and historical mechanisms shaping the evolutionary history of warm-temperate fish species. Using the genetic variation in the mitochondrial DNA Control Region and eight nuclear microsatellite DNA loci, we identified the presence of two highly divergent populations in a vagile and warm-temperate fish species, Atractoscion aequidens, across the Benguela region. The geographical distributions of the two populations, on either side of the perennial upwelling cell, suggest a strong correlation between the oceanographic features of the system and the breakdown of gene flow within this species. Genetic divergence (mtDNA φ ST = 0.902, microsatellite F ST = 0.055: probability of genetic homogeneity for either marker = p<0.001), absence of migrants (less than 1% per generation) between populations and coalescent estimates of time since most recent common ancestor suggest that the establishment of the main oceanographic features of the system (2 million years ago), particularly the strengthening and position of the perennial upwelling cell, is the most likely mechanism behind the observed isolation. Concordance between mitochondrial and nuclear genetic markers indicates that isolation and divergence of the northern and southern Benguela populations of A. aequidens occurred deep in the past and has continued to the present day. These findings suggest that the Benguela Current system may constitute an ancient and impermeable barrier to gene flow for warm-temperate fish species.