Responses of population structure and genomic diversity to climate change and fishing pressure in a pelagic fish.

The responses of marine species to environmental changes and anthropogenic pressures (e.g., fishing) interact with ecological and evolutionary processes that are not well understood. Knowledge of changes in the distribution range and genetic diversity of species and their populations into the future is essential for the conservation and sustainable management of resources. Almaco jack (Seriola rivoliana) is a pelagic fish with high importance to fisheries and aquaculture in the Pacific Ocean. In this study, we assessed contemporary genomic diversity and structure in loci that are putatively under selection (outlier loci) and determined their potential functions. Using a combination of genotype-environment association, spatial distribution models, and demogenetic simulations, we modeled the effects of climate change (under three different RCP scenarios) and fishing pressure on the species' geographic distribution and genomic diversity and structure to 2050 and 2100. Our results show that most of the outlier loci identified were related to biological and metabolic processes that may be associated with temperature and salinity. The contemporary genomic structure showed three populations-two in the Eastern Pacific (Cabo San Lucas and Eastern Pacific) and one in the Central Pacific (Hawaii). Future projections suggest a loss of suitable habitat and potential range contractions for most scenarios, while fishing pressure decreased population connectivity. Our results suggest that future climate change scenarios and fishing pressure will affect the genomic structure and genotypic composition of S. rivoliana and lead to loss of genomic diversity in populations distributed in the eastern-central Pacific Ocean, which could have profound effects on fisheries that depend on this resource.

Las respuestas de las especies marinas ante los cambios ambientales y presiones antropogénicas (por ejemplo, la sobrepesca) interactúan con procesos ecológicos y evolutivos que no se comprenden bien. El conocimiento del cambio en el rango de distribución y la diversidad genética de las especies y sus poblaciones en el futuro es fundamental para la conservación y gestión sostenible de los recursos. El jurel (Seriola rivoliana) es un pez pelágico de gran importancia para la pesca y la acuicultura en el Océano Pacífico. En este estudio, evaluamos la diversidad y estructura genómica contemporánea en loci que supuestamente están bajo selección (loci atípicos) y determinamos sus funciones potenciales. Se utilizó la combinación de métodos de asociación genotipo-ambiente, modelos de distribución espacial y simulaciones demogenéticas, para modelar los efectos del cambio climático (bajo tres escenarios RCP diferentes) y presión de pesca sobre la distribución geográfica de la especie, la diversidad y estructura genómica para los años 2050 y 2100. Nuestros resultados mostraron que la mayoría de los loci atípicos están relacionados con procesos biológicos y metabólicos que pueden estar asociados con la temperatura y la salinidad. La estructura genómica contemporánea mostró tres poblaciones: dos en el Pacífico oriental (Cabo San Lucas y el Pacífico oriental) y una en el Pacífico central (Hawai). Las proyecciones futuras sugieren una pérdida de hábitat idóneo y posibles contracciones del área de distribución para la mayoría de los escenarios, mientras que la presión de la pesca redujo la conectividad de las poblaciones. Nuestros resultados sugieren que los escenarios de cambio climático y la presión pesquera afectarán la estructura genómica y la composición genotípica de S. rivoliana y conducirán a la pérdida de diversidad genómica en las poblaciones distribuidas en el Océano Pacífico centro-oriental, lo que podría tener efectos en las pesquerías que dependen de este recurso.

Venom comparisons of endemic and micro-endemic speckled rattlesnakes Crotalus mitchellii, C. polisi and C. thalassoporus from Baja California Peninsula.

A high diversity of rattlesnake species can be found in the Baja California peninsula and the island of the Gulf of California, nevertheless, their venom has been poorly evaluated. The aim of this work was to present the first characterization of endemic Crotalus mitchellii, micro endemic C. polisi and C. thalassoporus venoms. All samples provoke human plasma coagulation showing doses in the rank of 2.3-41.0 µg and also produce rapid hydrolysis of the alpha chain of bovine fibrinogen while the beta chain is attacked at larger incubation periods by C. polisi and especially by C. thalassoporus. Phospholipase activity ranging from 23.2 to 173.8 U/mg. The venoms of C. thalassoporus and C. polisi show very high hemorrhagic activity (from 0.03 to 0.31 µg). A total of 130 toxin-related proteins were identified and classified into ten families. Crotalus mitchellii venom was characterized by high abundance of crotoxin-like and other phospholipase proteins (34.5%) and serine proteinases (29.8%). Crotalus polisi showed a similar proportion of metalloproteinases (34%) and serine proteinases (22.8%) components with important contribution of C-type lectins (14.3%) and CRiSP (14.0%) proteins. Venom of C. thalassoporus is dominated by metalloproteases that amount to more than 66% of total toxin proteins. These results provide a foundation for comprehending the biological, ecological and evolutionary significance of venom composition of speckled rattlesnake from the Baja California peninsula.

The queen conch mitogenome: intra- and interspecific mitogenomic variability in Strombidae and phylogenetic considerations within the Hypsogastropoda.

Aliger gigas is an economically important and vulnerable marine species. We present a new mitogenome of A. gigas from the Mexican Caribbean and use the eight publicly available Strombidae mitogenomes to analyze intra- and interspecific variation. We present the most complete phylogenomic understanding of Hypsogastropoda to date (17 superfamilies, 39 families, 85 genera, 109 species) to revisit the phylogenetic position of the Stromboidea and evaluate divergence times throughout the phylogeny. The A. gigas mitogenome comprises 15,460 bp including 13 PCGs, 22 tRNAs, and two rRNAs. Nucleotide diversity suggested divergence between the Mexican and Colombian lineages of A. gigas. Interspecific divergence showed high differentiation among Strombidae species and demonstrated a close relationship between A. gigas and Strombus pugilis, between Lambis lambis and Harpago chiragra, and among Tridentarius dentatus/Laevistrombus canarium/Ministrombus variabilis. At the intraspecific level, the gene showing the highest differentiation is ATP8 and the lowest is NAD4L, whereas at the interspecific level the NAD genes show the highest variation and the COX genes the lowest. Phylogenomic analyses confirm that Stromboidea belongs in the non-Latrogastropoda clade and includes Xenophoridea. The phylogenomic position of other superfamilies, including those of previously uncertain affiliation, is also discussed. Finally, our data indicated that Stromboidea diverged into two principal clades in the early Cretaceous while Strombidae diversified in the Paleocene, and lineage diversification within A. gigas took place in the Pleistocene.

Proteomic comparison of adult and juvenile Santa Catalina rattlesnake (Crotalus catalinensis) venom.

Rattlesnake's venom constitutes an important ecological trait that dynamically changes over time. Venoms of adult and juvenile rattleless rattlesnakes, Crotalus catalinensis, an endemic insular species from the Gulf of California, were compared by electrophoretic profile, fibrinogenolytic activity, and proteomic composition to assess ontogenetic variability. The SDS-PAGE profiles show important differences at 12, 22, and 45 kDa, which were prominent in adult samples and absent in juvenile samples, while bands around 20, 25, and 70 kDa are almost absent in adults. Both venoms hydrolyze Aa and Bb chains of fibrinogen generating different patterns of degradation products. This activity was partially inhibited by EDTA and PMSF and completely abolished only in the presence of both inhibitors. More than 260 proteins were identified and quantified in both venoms by proteomic analysis. Metalloproteinases (more than 60%), serine proteinases (14.5% in adult venom and 17.7% in juvenile venom), and C-type lectins (7.1 and 5.9%) represent the three most abundant toxin-related protein families. Bradykinin inhibitor peptides and L-amino acid oxidases were not detected in juvenile venom. A protein-specific comparison shows that adult and juvenile venom share about 30.5% of total toxin-related proteins, while 32% and 35% are exclusively present in adult and juvenile venoms, respectively. This work represents one of the first efforts to understand phenotypic diversity in the venom composition of insular rattlesnake species from Mexico.

Genetic diversity and structure of circumtropical almaco jack, Seriola rivoliana: tool for conservation and management.

The almaco jack, Seriola rivoliana, is a circumtropical pelagic fish of importance both in commercial fisheries and in aquaculture. To understand levels of genetic diversity within and among populations in the wild, population genetic structure and the relative magnitude of migration were assessed using mtDNA sequence data and single nucleotide polymorphisms (SNPs) from individuals sampled from locations in the Pacific and Atlantic Oceans. A total of 25 variable sites of cytochrome c oxidase subunit 1 and 3678 neutral SNPs were recovered. Three genetic groups were identified, with both marker types distributed in different oceanic regions: Pacific-1 in central Pacific, Pacific-2 in eastern Pacific and Atlantic in western Atlantic. Nonetheless, the analysis of SNP identified a fourth population in the Pacific coast of Baja California Sur, Mexico (Pacific-3), whereas that of mtDNA did not. This mito-nuclear discordance is likely explained by a recently diverged Pacific-3 population. In addition, two mtDNA haplogroups were found within the western Atlantic, likely indicating that the species came into the Atlantic from the Indian Ocean with historical gene flow from the eastern Pacific. Relative gene flow among ocean basins was low with r m < 0.2, whereas in the eastern Pacific it was asymmetric and higher from south to north (r m > 0.79). The results reflect the importance of assessing genetic structure and gene flow of natural populations for the purposes of sustainable management.

Adapterama I: universal stubs and primers for 384 unique dual-indexed or 147,456 combinatorially-indexed Illumina libraries (iTru & iNext).

Massively parallel DNA sequencing offers many benefits, but major inhibitory cost factors include: (1) start-up (i.e., purchasing initial reagents and equipment); (2) buy-in (i.e., getting the smallest possible amount of data from a run); and (3) sample preparation. Reducing sample preparation costs is commonly addressed, but start-up and buy-in costs are rarely addressed. We present dual-indexing systems to address all three of these issues. By breaking the library construction process into universal, re-usable, combinatorial components, we reduce all costs, while increasing the number of samples and the variety of library types that can be combined within runs. We accomplish this by extending the Illumina TruSeq dual-indexing approach to 768 (384 + 384) indexed primers that produce 384 unique dual-indexes or 147,456 (384 × 384) unique combinations. We maintain eight nucleotide indexes, with many that are compatible with Illumina index sequences. We synthesized these indexing primers, purifying them with only standard desalting and placing small aliquots in replicate plates. In qPCR validation tests, 206 of 208 primers tested passed (99% success). We then created hundreds of libraries in various scenarios. Our approach reduces start-up and per-sample costs by requiring only one universal adapter that works with indexed PCR primers to uniquely identify samples. Our approach reduces buy-in costs because: (1) relatively few oligonucleotides are needed to produce a large number of indexed libraries; and (2) the large number of possible primers allows researchers to use unique primer sets for different projects, which facilitates pooling of samples during sequencing. Our libraries make use of standard Illumina sequencing primers and index sequence length and are demultiplexed with standard Illumina software, thereby minimizing customization headaches. In subsequent Adapterama papers, we use these same primers with different adapter stubs to construct amplicon and restriction-site associated DNA libraries, but their use can be expanded to any type of library sequenced on Illumina platforms.

Red Queen revisited: Immune gene diversity and parasite load in the asexual Poecilia formosa versus its sexual host species P. mexicana.

In accordance with the Red Queen hypothesis, the lower genotypic diversity in clonally reproducing species should make them easier targets for pathogen infection, especially when closely related sexually reproducing species occur in close proximity. We analyzed two populations of clonal P. formosa and their sexual parental species P. mexicana by correlating individual parasite infection with overall and immune genotype. Our study revealed lower levels of overall genotypic diversity and marginally fewer MHC class I alleles in P. formosa individuals compared to sexually reproducing P. mexicana. Parasite load, however, differed only between field sites but not between species. We hypothesize that this might be due to slightly higher genotypic diversity in P. formosa at the innate immune system (toll like receptor 8) which is likely due to the species' hybrid origin. In consequence, it appears that clonal individuals do not necessarily suffer a disadvantage compared to sexual individuals when fighting parasite infection.

Phylogeography and Ecological Niche Modeling of the Desert Iguana (Dipsosaurus dorsalis, Baird & Girard 1852) in the Baja California Peninsula.

Understanding the factors that explain the patterns of genetic structure or phylogeographic breaks at an intraspecific level is key to inferring the mechanisms of population differentiation in its early stages. These topics have been well studied in the Baja California region, with vicariance and the dispersal ability of individuals being the prevailing hypothesis for phylogeographic breaks. In this study, we evaluated the phylogeographic patterns in the desert iguana (Dipsosaurus dorsalis), a species with a recent history in the region and spatial variation in life history traits. We analyzed a total of 307 individuals collected throughout 19 localities across the Baja California Peninsula with 15 microsatellite DNA markers. Our data reveal the existence of 3 geographically discrete genetic populations with moderate gene flow and an isolation-by-distance pattern presumably produced by the occurrence of a refugium in the Cape region during the Pleistocene Last Glacial Maximum. Bayesian methods and ecological niche modeling were used to assess the relationship between population genetic structure and present and past climatic preferences of the desert iguana. We found that the present climatic heterogeneity of the Baja California Peninsula has a marked influence on the population genetic structure of the species, suggesting that there are alternative explanations besides vicariance. The information obtained in this study provides data allowing a better understanding of how historical population processes in the Baja California Peninsula can be understood from an ecological perspective.

Assessing population-level morphometric variation of the Mountain Mullet Agonostomus monticola (Teleostei: Mugilidae) across its Middle American distribution

Population-level morphometric variation of the Mountain Mullet (Agonostomus monticola) was assessed in 419 adult specimens from 25 sample sites (river basins) across its Middle American distribution (Pacific and Atlantic-Caribbean drainages). This analysis was based on 36 standardized linear measurements and 19 landmarks on geometric morphometrics approach. Discriminant function analysis (DFA) revealed 19 linear morphological characters with significant variation among groups. Geometrically, the most notable changes were associated to the curvature of the frontal region of the head, the anterior and posterior insertion of the first dorsal and anal fins. The resulting grouping based on the DFA and geometric morphometrics techniques (Pacific-A, Pacific-B and NE México-Caribbean) were similar to those previously recovered by genetic techniques, where the Pacific-B (Ayuquila river basin) was the most different group. Our results provide morphological evidence for considering Agonostomus monticola as a complex of evolutionary entities, represented by two forms in the Pacific Ocean and another in the Atlantic Ocean.(AU)

La variación morfométrica de poblaciones de la lisa de montaña Agonostomus monticola fue evaluada en 419 especímenes adultos recolectados en 25 sitios (cuencas) a través de su distribución mesoamericana (Pacífico, Atlántico y cuencas del Caribe). El análisis fue basado en 36 medidas lineales estandarizadas y 19 puntos de referencia basados en morfometría geométrica. El análisis de función discriminante (AFD) reveló 19 caracteres morfométricos con variación significativa entre grupos. Geométricamente, los cambios más notables estuvieron asociados con la curvatura de la región frontal de la cabeza y la inserción anterior y posterior de la primera aleta dorsal y de la aleta anal. Los agrupamientos resultantes del AFD y del análisis de morfometría geométrica (Pacífico-A, Pacífico-B y NE México-Caribe) fueron similares con los previamente definidos mediante técnicas genéticas. El grupo Pacífico-B (cuenca de Ayuquila) fue el más disímil. Nuestros resultados proveen evidencia morfológica para considerar a Agonostomus monticola como un complejo de entidades evolutivas, representadas por dos formas en la cuenca del océano Pacífico y una forma en la cuenca del océano Atlántico.(AU)

Panmixia in a Critically Endangered Fish: The Totoaba (Totoaba macdonaldi) in the Gulf of California.

Conservation of the evolutionary legacy of endangered species is a key component for long-term persistence. Totoaba is a long-lived fish endemic to the Gulf of California and is considered critically endangered. There is currently a debate concerning its conservation status and whether it can be used as a fishery resource. Unfortunately, basic information on biological and genetic population structure of the species is lacking. We sampled 313 individuals and employed 16 microsatellite loci and 3 mitochondrial DNA markers (16S, 547 pb; COI, 619 pb; control region, 650 pb) to assess population structure and demography of totoaba in the Gulf of California, with samples from locations that encompass nearly all of its recognized geographic distribution. We could not reject a hypothesis of panmixia for totoaba, using nuclear or mitochondrial markers. Demographic analysis of mtDNA suggests a sudden population expansion model. The results have important implications for totoaba conservation because poaching is a significant conservation challenge and could have additive negative effects over the single population of totoaba in the Gulf of California.

Phylogeography of endemic Xantus' hummingbird (Hylocharis xantusii) shows a different history of vicariance in the Baja California Peninsula.

Studies of phylogeographic patterns provide insight into the processes driving lineage divergence in a particular region. To identify the processes that caused phylogeographic breaks, it is necessary to use historical information and a set of appropriate molecular data to explain current patterns. To understand the influence of geological or ecological processes on the phylogeography of the only species of hummingbird endemic to the Baja California Peninsula, Hylocharis xantusii, mitochondrial DNA sequences of three concatenated genes (Cyt-b, COI and ND2; 2297bp in total) in 100 individuals were analyzed. The spatial analyses of genetic variation showed phylogeographic structure consisting of a north, central and south regions. According to estimated divergence times, two vicariant events are supported, permanent separation of the peninsula and formation of the Gulf of California at 5mya and temporary isolation of the southern region at the Isthmus of La Paz at 3mya. The temporal frame of genetic differentiation of intraspecific haplotypes indicates that 90% of haplotypes diverged within the last 500,000years, with a population expansion 80,000years ago. Only four haplotypes diverged ∼2.2 my and occurred in the south (Hxan_36, 38 and 45), and north (Hxan_45 and 56) regions; only haplotype 45 is shared between south and north populations. These regions also have the most recent haplotypes from 12,500 to 16,200years ago, and together with high levels of genetic diversity, we suggest two refuge areas, the Northern and Southern regions. Our results indicate that the phylogeographic pattern first results from vicariance processes, then is followed by historical and recent climate fluctuations that influenced conditions on the peninsula, and it is also related to oases distribution. This study presents the first investigation of phylogeography of the peninsular' endemic Xantus' hummingbird.

Do relaxed selection and habitat temperature facilitate biased mitogenomic introgression in a narrowly endemic fish?

Introgression might be exceptionally common during the evolution of narrowly endemic species. For instance, in the springs of the small and isolated Cuatro Ciénegas Valley, the mitogenome of the cichlid fish Herichthys cyanoguttatus could be rapidly introgressing into populations of the trophically polymorphic H. minckleyi. We used a combination of genetic and environmental data to examine the factors associated with this mitochondrial introgression. A reduced representation library of over 6220 single nucleotide polymorphisms (SNPs) from the nuclear genome showed that mitochondrial introgression into H. minckleyi is biased relative to the amount of nuclear introgression. SNP assignment probabilities also indicated that cichlids with more hybrid ancestry are not more commonly female providing no support for asymmetric backcrossing or hybrid-induced sex-ratio distortion in generating the bias in mitochondrial introgression. Smaller effective population size in H. minckleyi inferred from the SNPs coupled with sequences of all 13 mitochondrial proteins suggests that relaxed selection on the mitogenome could be facilitating the introgression of "H. cyanoguttatus" haplotypes. Additionally, we showed that springs with colder temperatures had greater amounts of mitochondrial introgression from H. cyanoguttatus. Relaxed selection in H. minckleyi coupled with temperature-related molecular adaptation could be facilitating mitogenomic introgression into H. minckleyi.

Entire mitochondrion genome sequence of the Desert Pupfish, Cyprinodon macularius Baird & Girard, 1853.

The complete mitochondrial genome sequence of the Desert Pupfish, Cyprinodon macularius (Gene accession number KM985373) has a length of 16,940 bp, and the arrangement consisted of 13 protein-coding genes, 2 ribosomal RNA (rRNA) genes and 22 transfer RNA, which are similar to other known mitogenomes for the family Cyprinodontidae.

Lionfish, Pterois volitans Linnaeus 1758, the complete mitochondrial DNA of an invasive species.

The lionfish, Pterois volitans, native from the Indo-Pacific, has been found in Atlantic and Caribbean waters and is considered as an invasive species. Here we sequence its mitogenome (Genbank accession number KJ739816), which has a total length of 16,500 bp, and the arrangement consist of 13 protein-coding genes, 2 ribosomal RNA (rRNA) genes and 22 transfer RNA similar to other Pteroinae subfamily (family Scorpaenidae). This mitogenome will be useful for phylogenetic and population genetic studies of this invasive species.

The complete mitochondrial DNA of the tropical gar (Atractosteus tropicus).

The mitogenome of the tropical gar, Atractosteus tropicus, (GeneBank accession number KJ531198) has a total length of 16,280 bp, and the arrangement consist of 13 protein-coding genes, 2 ribosomal RNA (rRNA) genes and 22 transfer RNA similar to other Lepisosteidae family mitogenomes.

The complete mitochondrial DNA of the bull shark (Carcharhinus leucas).

The bull shark mitochondrial structure is similar to that of other elasmobranchs; it has a total length of 16,100 bp, the base composition of the genomes was as follows: A (31.35%), T (31.35%), C (24.38%) and G (12.90%). It contains 13 protein-coding genes and 23 tRNA genes. The tRNA genes range from 70-72 bp. Gene order is the same as in other vertebrates and teleosts.

The complete mitochondrial DNA of endemic Eastern Pacific coral (Porites panamensis).

The mitogenome of the endemic coral Porites panamensis (Genbank accession number KJ546638) has a total length of 18,628 bp, and the arrangement consist of 13 protein-coding genes, 2 ribosomal RNA (rRNA) genes and 2 transfer RNA (tRNA) genes. Gene order was equal to other scleractinian coral mitogenomes.

The complete mitochondrial DNA of the silky shark (Carcharhinus falciformis).

The silky shark mitogenome (GeneBank accession number KF801102) has a total length of 17,774 bp, the base composition of the genomes was as follows: A (31.36%), T (30.18%), C (25.27%) and G (13.17%), which demonstrated an A + T-rich feature (61.64%), similar to other elasmobranch mitogenomes. The mitochondrial genome contained 13 protein-coding genes and 23 tRNA genes. The tRNA genes ranged from 70 to 72 bp. The gene order was the same as in other vertebrates and teleosts.

Genetic variability between complete mitochondrion genomes of the sablefish, Anoplopoma fimbria (Pallas, 1814).

The complete mitochondrial genome of the sablefish, Anoplopoma fimbria (Genbank accession KP777542) is 16,507 bp in size and contains the typical 37 genes (13 protein-coding, 2 ribosomal RNA, and 22 transfer RNA) found in teleosts mitogenomes. The genome varies in 118 positions with respect to another mitogenome sablefish specimen.

The complete mitochondrial DNA of white shark (Carcharodon carcharias) from Isla Guadalupe, Mexico.

The Isla Guadalupe white shark mitochondrial structure is similar to the one previously reported for a white shark individual from Taiwan with a total length of 16,745 and 16,742 bp respectively; the base composition of the genomes was as follow A (30.60%), T (28.67%), C (26.86%) and G (13.87%), contains 13 protein-coding genes and 24 tRNA genes and the non-coding control region. The tRNA genes range from 70-72 bp. Gene order is the same as in other vertebrates and teleosts.