Embiotoca Jacksoni Research Articles

A high-quality reference genome of the kelp surfperch, Brachyistius frenatus (Embiotocidae), a wide-ranging Eastern Pacific reef fish with no pelagic larval stage.

The surfperches (family Embiotocidae) are a unique group of mostly marine fishes whose phylogenetic position within the Ovalentaria clade (Percomorpha) is still unresolved. As a result of their viviparity and lack of a dispersive larval stage, surfperches are an excellent model for the study of speciation, gene flow, and local adaptation in the ocean. They are also the target of an immensely popular recreational fishery. Very few high-quality molecular resources, however, are available for this group and only for a single species. Here, we describe a highly complete reference genome for the kelp surfperch, Brachyistius frenatus, assembled using a combination of short-read (Illumina, ~47× coverage) and long-read (Oxford Nanopore Technologies, ~27× coverage) sequencing. The 596 Mb assembly has a completeness level of 98.1% (BUSCO), a contig N50 of 2.6 Mb (n = 56), and a contig N90 of 406.6 kb (n = 293). Comparative analysis revealed a high level of synteny between B. frenatus and its close relative, Embiotoca jacksoni. This assembly will serve as a valuable molecular resource upon which future evolutionary dynamics research will build, such as the investigation of local adaptation and the genomic potential for climate adaptation in wild populations.

Upwelling-level acidification and pH/pCO2 variability moderate effects of ocean acidification on brain gene expression in the temperate surfperch, Embiotoca jacksoni.

Acidification‐induced changes in neurological function have been documented in several tropical marine fishes. Here, we investigate whether similar patterns of neurological impacts are observed in a temperate Pacific fish that naturally experiences regular and often large shifts in environmental pH/pCO2. In two laboratory experiments, we tested the effect of acidification, as well as pH/pCO2 variability, on gene expression in the brain tissue of a common temperate kelp forest/estuarine fish, Embiotoca jacksoni. Experiment 1 employed static pH treatments (target pH = 7.85/7.30), while Experiment 2 incorporated two variable treatments that oscillated around corresponding static treatments with the same mean (target pH = 7.85/7.70) in an eight‐day cycle (amplitude ± 0.15). We found that patterns of global gene expression differed across pH level treatments. Additionally, we identified differential expression of specific genes and enrichment of specific gene sets (GSEA) in comparisons of static pH treatments and in comparisons of static and variable pH treatments of the same mean pH. Importantly, we found that pH/pCO2 variability decreased the number of differentially expressed genes detected between high and low pH treatments, and that interindividual variability in gene expression was greater in variable treatments than static treatments. These results provide important confirmation of neurological impacts of acidification in a temperate fish species and, critically, that natural environmental variability may mediate the impacts of ocean acidification.

Reference Genome of the Black Surfperch, Embiotoca jacksoni (Embiotocidae, Perciformes), a California Kelp Forest Fish That Lacks a Pelagic Larval Stage.

Surfperches (Family Embiotocidae) are viviparous temperate reef fishes that brood their young. This life history trait translates into limited dispersal, strong population structure, and an unusually strong potential for local adaptation in a marine fish. As part of the California Conservation Genomics Project (CCGP), we sequenced the genome of the Black Surfperch, Embiotoca jacksoni, to establish a genomic model for understanding phylogeographic patterns of marine organisms in California. These patterns, in turn, may inform the design of marine protected areas using dispersal models based on genomic data. The genome of E. jacksoni is typical of marine fishes at less than 1Gb (genome size = 635 Mb), and our assembly is near-chromosome level (contig N50 = 6.5Mb, scaffold N50 = 15.5 Mb, BUSCO = 98.1%). Within the context of the CCGP, the genome will be used as a reference for future whole genome resequencing projects aimed at enhancing our knowledge of the population structure of the species, and efficacy of Marine Protected Areas across the state.

External reproductive structures of male Surfperches (Embiotocidae): Urogenital papilla.

Fishes exhibit a dynamic array of reproductive diversity. Among the various forms of reproduction, internal fertilization has evolved at least 13 times and has been observed in 2-3% of teleost species, half of which are marine. Internal fertilization has led to the evolution of male intromittent organs to aid in sperm transfer during copulation. The intromittent organs of poeciliids have been widely investigated, but little research has focused on the intromittent organs of marine fishes. The surfperches are internally fertilizing, viviparous fishes with a ventrally located papilla. In this article, the external morphology of 19 Embiotocidae species was examined. Additionally, paraffin histology was used to investigate the walleye surfperch (Hyperprosopon argenteum), black perch (Embiotoca jacksoni), and dwarf perch (Micrometrus minimus) papilla to aid in the identification of tissue composition to determine its function. External morphology was documented via macro photography and males were dissected to observe the relationship between the testes, spermatic duct, and papilla. We provide histological evidence that the urogenital papilla is directly connected to the spermatic duct and testis and likely involved in spermatozeugmata transfer. Our research also determined that the papillae were composed of both urinary and reproductive tissues, thus we propose the papilla be referred to as a urogenital papilla. Our study contributes to an overall understanding of intromittent organs of marine fishes, particularly in the surfperches, which has not been previously documented.

Local adaptation of antipredator behaviors in populations of a temperate reef fish.

The temperament of animals can vary among individuals and among populations, but it is often unclear whether spatial variation in temperament is the result of acclimation to local environmental conditions or genetic adaptation to spatial differences in natural selection. This study tested whether populations of a marine fish that experience different levels of mortality and fishing exhibited local adaptation in behaviors related to predator avoidance and evasion. First, we measured variation in reactivity to perceived risk in wild populations of black surfperch (Embiotoca jacksoni). We compared flight initiation distances (FID) between populations with significantly different mortality rates. After finding that FID values were substantially lower in the low-risk locations, we tested for local adaptation by rearing lab-born offspring from both high- and low-risk populations in a common environment before measuring their behavior. Lab-reared offspring from high- and low-risk populations exhibited significant differences in several behaviors related to reactivity. Between 23 and 43% of the total variation in behaviors we measured could be attributed to source population. These results thus suggest that a substantial amount of spatial variation in behaviors related to predator evasion may represent local adaptation. In addition, behaviors we measured had an average, broad-sense heritability of 0.24, suggesting that the behavioral tendencies of these populations have some capacity to evolve further in response to any changes in selection.

Geographic variation in demography of black perch (Embiotoca jacksoni): Effects of density, food availability, predation, and fishing

It is well known that demographic rates such as growth and mortality may vary among populations, but the degree of variation in demography is often unknown, especially when considering multiple populations at large spatial scales (e.g., across hundreds of kilometers). Likewise, of the many factors that may affect demography, it is often unknown which are the major factors responsible for spatial variation in demographic rates. In this study, we estimated rates of growth and examined age distributions within nine populations of black perch (Embiotoca jacksoni) distributed across ~350 km of coastline. We tested whether spatial variation in demography was associated with several explanatory variables including population density, predator density, food availability, and fishing activity. Our study revealed a substantial amount of spatial variation in demographic rates. Among-population variation in growth accounted for 55% of the total variation, and the coefficient of variation for mean age within a population was 27%, suggesting substantial variation in mortality. Spatial variation in growth was most sensitive to variation in food availability and mean age was lowest at locations with high levels of spearfishing activity. Although the fishery for black perch is not a major one, fishing mortality rates may be very high in some areas. Overall, our results shed light on the ecological forces that shape demographic variation of this species, and suggest that fishing mortality may have a major influence on the dynamics of perch populations.

Effects of size and sex on the courting success and foraging behaviour of Embiotoca jacksoni.

To test life-history theory that body size and sex should influence how animals allocate time to foraging versus reproductive activities, we measured the effects of size and sex on courting success and foraging behaviour of black surfperch Embiotoca jacksoni off Santa Catalina Island, southern California. Observations of focal fish were made while snorkelling, during which the length of each fish (estimated to the nearest cm), total duration of courting encounters and foraging rates were recorded. We made observations during and outside the mating season. Courtship occurred only between pairs and its duration increased with the size of both the male and female. Although males would court females that were smaller or larger than themselves, pairs that were closely matched in size had long courting sessions, whereas those that differed considerably in size courted only briefly. Small fish foraged more than larger fish, both during and outside the mating season. Males and females foraged at similar rates outside of the mating season, but during the mating season males reduced their foraging rates to less than half that seen outside of the mating season, whereas females continued to forage at the same rate. This decrease in foraging rate of males during the mating season was seen in all sizes of males but was proportionally greatest in the largest males. These observations indicate that males trade off time spent on foraging for time spent courting during the mating season, whereas females do not.

The complete mitochondrial genome of the black surfperch, Embiotoca jacksoni: Selection and substitution rates among surfperches (Embiotocidae)

The complete 16,515bp nucleotide sequence of the mitochondrial genome was determined for the black surfperch, Embiotoca jacksoni (Perciformes: Embiotocidae). The black surfperch mitochondrial genome contains 13 protein-coding genes, two ribosomal RNA genes, 22 transfer RNA genes, and the non-coding control region (D-loop), the gene order of which is identical to that observed in most vertebrates. The protein-coding gene sequences of E. jacksoni mitochondrial DNA were compared with two other embiotocid surfperches with available complete mitochondrial genomes, Cymatogaster aggregata and Ditrema temminckii. Across all mitochondrial protein-coding genes in surfperches the weighted average substitution rate was 2.079% per My and average dN/dS ratios for each protein-coding gene ranged from 0.016 in CytB to 0.608 in ND3. Substitution rates and dN/dS ratios were relatively high for ATP8 compared to other protein-coding genes. Although most protein-coding genes showed signals of purifying selection, we found evidence for positive selection in ND3 in E. jacksoni.

Genetic diversity affects the strength of population regulation in a marine fish

AbstractVariation is an essential feature of biological populations, yet much of ecological theory treats individuals as though they are identical. This simplifying assumption is often justified by the perception that variation among individuals does not have significant effects on the dynamics of whole populations. However, this perception may be skewed by a historic focus on studying single populations. A true evaluation of the extent to which among‐individual variation affects the dynamics of populations requires the study of multiple populations. In this study, we examined variation in the dynamics of populations of a live‐bearing, marine fish (black surfperch; Embiotoca jacksoni). In collaboration with an organization of citizen scientists (Reef Check California), we were able to examine the dynamics of eight populations that were distributed throughout ~700 km of coastline, a distance that encompasses much of this species’ range. We hypothesized that genetic variation within a local population would be related to the intensity of competition and to the strength of population regulation. To test this hypothesis, we examined whether genetic diversity (measured by the diversity of mitochondrial DNA haplotypes) was related to the strength of population regulation. Low‐diversity populations experienced strong density dependence in population growth rates and population sizes were regulated much more tightly than they were in high‐diversity populations. Mechanisms that contributed to this pattern include links between genetic diversity, habitat use, and spatial crowding. On average, low‐diversity populations used less of the available habitat and exhibited greater spatial clustering (and more intense competition) for a given level of density (measured at the scale of the reef). Although the populations we studied also varied with respect to exogenous characteristics (habitat complexity, densities of predators, and interspecific competitors), none of these characteristics was significantly related to the strength of population regulation. In contrast, an endogenous characteristic of the population (genetic diversity) explained 77% of the variation in the strength of population regulation (95% CI: 27–94%). Our results suggest that the genetic and phenotypic composition of populations can play a major role in their dynamics.

Genetic diversity affects the strength of population regulation in a marine fish.

Variation is an essential feature of biological populations, yet much of ecological theory treats individuals as though they are identical. This simplifying assumption is often justified by the perception that variation among individuals does not have significant effects on the dynamics of whole populations. However, this perception may be skewed by a historic focus on studying single populations. A true evaluation of the extent to which among-individual variation affects the dynamics of populations requires the study of multiple populations. In this study, we examined variation in the dynamics of populations of a live-bearing, marine fish (black surfperch; Embiotoca jacksoni). In collaboration with an organization of citizen scientists (Reef Check California), we were able to examine the dynamics of eight populations that were distributed throughout approximately 700 km of coastline, a distance that encompasses much of this species' range. We hypothesized that genetic variation within a local population would be related to the intensity of competition and to the strength of population regulation. To test this hypothesis, we examined whether genetic diversity (measured by the diversity of mitochondrial DNA haplotypes) was related to the strength of population regulation. Low-diversity populations experienced strong density dependence in population growth rates and population sizes were regulated much more tightly than they were in high-diversity populations. Mechanisms that contributed to this pattern include links between genetic diversity, habitat use, and spatial crowding. On average, low-diversity populations used less of the available habitat and exhibited greater spatial clustering (and more intense competition) for a given level of density (measured at the scale of the reef). Although the populations we studied also varied with respect to exogenous characteristics (habitat complexity, densities of predators, and interspecific competitors), none of these characteristics was significantly related to the strength of population regulation. In contrast, an endogenous characteristic of the population (genetic diversity) explained 77% of the variation in the strength of population regulation (95% CI: 27-94%). Our results suggest that the genetic and phenotypic composition of populations can play a major role in their dynamics.

Exposure to bloom-like concentrations of two marine Synechococcus cyanobacteria (strains CC9311 and CC9902) differentially alters fish behaviour.

Coastal California experiences large-scale blooms of Synechococcus cyanobacteria, which are predicted to become more prevalent by the end of the 21st century as a result of global climate change. This study investigated whether exposure to bloom-like concentrations of two Synechococcus strains, CC9311 and CC9902, alters fish behaviour. Black perch (Embiotoca jacksoni) were exposed to Synechococcus strain CC9311 or CC9902 (1.5 × 10(6) cells ml(-1)) or to control seawater in experimental aquaria for 3 days. Fish movement inside a testing arena was then recorded and analysed using video camera-based motion-tracking software. Compared with control fish, fish exposed to CC9311 demonstrated a significant preference for the dark zone of the tank in the light-dark test, which is an indication of increased anxiety. Furthermore, fish exposed to CC9311 also had a statistically significant decrease in velocity and increase in immobility and they meandered more in comparison to control fish. There was a similar trend in velocity, immobility and meandering in fish exposed to CC9902, but there were no significant differences in behaviour or locomotion between this group and control fish. Identical results were obtained with a second batch of fish. Additionally, in this second trial we also investigated whether fish would recover after a 3 day period in seawater without cyanobacteria. Indeed, there were no longer any significant differences in behaviour among treatments, demonstrating that the sp. CC9311-induced alteration of behaviour is reversible. These results demonstrate that blooms of specific marine Synechococcus strains can induce differential sublethal effects in fish, namely alterations light-dark preference behaviour and motility.

Fish growth, reproduction, and tissue production on artificial reefs relative to natural reefs

Abstract The extent to which artificial reefs may be useful for mitigation of environmental impacts, fisheries management, and conservation depends in part upon how well the organisms that live on them fare. We tested whether fish living on artificial reefs were in similar condition (weight-at-length), grew, foraged, reproduced, and produced tissue at rates similar to those on natural reefs. We studied five artificial–natural reef pairs spread over >200 km in the Southern California Bight. Underwater visual transects were used to quantify density and size structure of four target species (Paralabrax clathratus, Paralabrax nebulifer, Semicossyphus pulcher, and Embiotoca jacksoni), which were also collected to measure foraging success, condition, growth, reproductive output, and tissue production. Generally, fish living on artificial reefs fared as well or better than those on natural reefs, with some exceptions. Semicossyphus pulcher fared better on artificial reefs, having higher foraging success, fecundity, densities, and tissue production. Embiotoca jacksoni grew faster on natural reefs, and P. nebulifer was in slightly better condition on natural reefs. Total fish tissue production tended to be higher on artificial reefs than on natural reefs, though this pattern was not evident on all reef pairs. Tissue production was positively correlated with the abundance of large boulders, which was higher on artificial reefs than natural reefs. The similar or greater production of fish tissue per cubic metre on artificial reefs relative to natural reefs indicates that these artificial habitats are valuable in producing fish biomass. Fish living on artificial reefs fared as well as those living on natural reefs, indicating that well-designed artificial reefs can be useful tools for mitigation, conservation, and fisheries management.

Shoaling preference and evidence for maintenance of sibling groups by juvenile black perch Embiotoca jacksoni

Group sizes in free-living juvenile black perch Embiotoca jacksoni were quantified and predictions of the hypothesis that such groups comprise sibling brood-mates were tested. Group sizes in the field were within the range of female brood sizes and often occurred close to each other but did not merge. In captivity, juveniles formed groups immediately after birth. In laboratory experiments, they also associated significantly more with chambers containing familiar members of their own brood than empty chambers but did not associate more with chambers containing similar-sized juveniles from a different brood. Juvenile E. jacksoni also associated significantly more with chambers containing familiar brood-mates than with chambers containing unfamiliar members of a different brood. The strength of this preference increased with the number of days fish had been together since birth. When two broods were placed in a large outdoor tank, all individuals from both broods directed significantly more aggressive acts towards members of the other brood than towards members of their own brood. While the relative effects of familiarity and relatedness cannot be completely separated in this viviparous species, associating with familiar individuals would facilitate the maintenance of sibling groups in the field.

The name of the father: conflict between Louis and Alexander Agassiz and theEmbiotocasurfperch radiation

The surfperch genus Embiotoca currently comprises two species, Embiotoca jacksoni, the black surfperch, and Embiotoca lateralis, the striped surfperch. Originally, however, Louis Agassiz described a third species in the genus Embiotoca, the rainbow surfperch, Embiotoca caryi. This latter name was changed by Louis' son, Alexander, to Hypsurus caryi, a name that remains valid. In this study, new molecular data (3545 bp of DNA from four mitochondrial and two nuclear DNA regions) indicated that the rainbow surfperch should be retained within the genus Embiotoca, a result consistent with recent morphological data. Adaptive radiation combined with sexual selection resulting in rapid morphological changes in the rainbow surfperch may have contributed to the conflicting position of this species.

Multiple paternity and competition in sympatric congeneric reef fishes,Embiotoca jacksoniandE. lateralis

The black surfperch Embiotoca jacksoni and the striped surfperch E. lateralis (Embiotocidae, Perciformes) are livebearing temperate reef fishes that live sympatrically over a large portion of their distribution range, where they exhibit strong ecological competition. In order to assess whether mating strategies reflect competition, we investigated multiple paternity in these two species in an area of sympatry. We sampled 24 pregnant females (12 for each species) in Monterey Bay, California, used microsatellite analysis and assessed paternity with the COLONY software. While broods are relatively small (12 to 36 offspring), they were always sired by multiple fathers (2 to 9), with no correlation between the size of a brood and the number of fathers. The number of sires for each brood was not significantly different between the two species (approximately 3.5 sires per brood). We tested the deviation from stochasticity of fathered offspring for each father in one brood. Results showed a significant deviation for both E. jacksoni and E. lateralis. However, this deviation was not found to be significant between species. The striking similarity in the dynamics of multiple paternity in these species, when sampled in sympatry, may result from several alternative scenarios, including phylogenetic inertia, reproductive behaviour, and ecological competition.

Isolation and characterization of 12 microsatellites from the black surfperch, Embiotoca jacksoni, a reef fish that lacks a pelagic larval phase

A set of 12 microsatellite markers was developed from Embiotoca jacksoni genomic DNA and tested for polymorphism using 64 individuals from two populations. All loci were polymorphic with a number of alleles ranging from two to 19 with expected heterozygosities ranging from 0.17 to 0.89. There was no evidence of linkage disequilibrium and all loci were in Hardy-Weinberg equilibrium, except for four loci in one population. High numbers of private alleles were consistent with strong population structure, and very limited dispersal. Six microsatellite markers successfully cross amplified and were polymorphic in closely related species, Embiotoca lateralis and Hyspurus caryi.

Life History and Courtship Behavior of Black Perch, Embiotoca jacksoni (Teleostomi: Embiotocidae), from Southern California

The black perch, Embiotoca jacksoni Agassiz, 1853, is a common reef fish associated with nearshore marine habitats of California, with the majority of the population occurring within the Southern California Bight. Black perch were collected throughout southern California from Santa Barbara to Carlsbad, including Santa Catalina Island, to determine their physical characteristics, growth, sex ratio, periodicity of reproduction, and length of gestation. Courtship observations were conducted using scuba along the King Harbor Breakwater in Redondo Beach, California, from January 2004 to December 2005 to verify periodicity of courting and associated reproductive behaviors. Specimens captured ranged from 75 to 220 mm standard length and from 18 to 487 g in total body weight. Seven age-classes were determined by otolith aging, with the growth rate tapering off after age-class one. Seventy percent of the individuals captured were from age-classes one to three. Growth rates did not differ between sexes. Mean monthly gonosomatic indexes for males peaked from July to November, with the highest mean occurring in October. Gestating females were found from December to May, with youngest gestating females being in age-class one. Courtship behaviors were observed within aggregations and in pairs from July to November, with males being the primary aggressors. Courtship postures occurred along the base of the reef, with pairs departing into caves for copulation. This study suggests that the black perch population within the Southern California Bight has different life history characteristics and reproductive timing than those in northern California.

The Reef Fish Assemblage of the Outer Los Angeles Federal Breakwater, 2002–2003

The conspicuous and cryptic fish assemblage of the Los Angeles Federal Breakwater was assessed from 2002 to 2003. Thirty-five species were observed or collected during the study period. The assemblage of cryptic fishes was composed primarily of a mix of Oregonian and San Diegan, species including snubnose sculpin (Orthonopias triacis), coralline sculpin (Artedius corallinus) and blackeye goby (Rhinogobiops nicholsii). The species composition of conspicuous fishes was approximately equal between taxa from these two provinces. Blacksmith (Chromis punctipinnis), black perch (Embiotoca jacksoni) and kelp bass (Paralabrax clathratus) dominated the assemblage of conspicuous fishes. Species composition reflects the localized cool temperature regime of the area and the high relief kelp forest habitat.

PHYLOGEOGRAPHY AND DEMOGRAPHY OF SYMPATRIC SISTER SURFPERCH SPECIES, EMBIOTOCA JACKSONI AND E. LATERALIS ALONG THE CALIFORNIA COAST: HISTORICAL VERSUS ECOLOGICAL FACTORS

With 18 closely related endemic species that radiated in a diversity of ecological niches, the California surfperches (Embiotocidae) species flock is a good candidate for the study of sympatric speciation. Resource partitioning has been suggested as an important driving force in the radiation of the surfperch family. Within the family, two congeneric sister species, Embiotoca jacksoni and E. lateralis, are known to compete strongly for a preferred single food resource and may be used as a model of ecological interactions for the family. Along the California coast, the distribution of the two species differs. Embiotoca jacksoni has a continuous range, whereas E. lateralis shows a disjunction with a distribution gap in the Southern California Bight. Two hypotheses may explain this disjunct distribution. Ecological competition may have displaced E. lateralis in favor of E. jacksoni. Alternatively, a common vicariant event may have separated the species into northern and southern populations, followed by secondary contact in E. jacksoni but not in E. lateralis. The two hypotheses predict different phylogeographic and demographic signatures. Using a combined phylogeographic and coalescent approach based on mitochondrial control region data, we show that vicariance can only account for a portion of the observed divergences. Our results are compatible with a significant role played by ecological competition in the southern range of the species.

PHYLOGEOGRAPHY AND DEMOGRAPHY OF SYMPATRIC SISTER SURFPERCH SPECIES, EMBIOTOCA JACKSONI AND E. LATERALIS ALONG THE CALIFORNIA COAST: HISTORICAL VERSUS ECOLOGICAL FACTORS

With 18 closely related endemic species that radiated in a diversity of ecological niches, the California surfperches (Embiotocidae) species flock is a good candidate for the study of sympatric speciation. Resource partitioning has been suggested as an important driving force in the radiation of the surfperch family. Within the family, two congeneric sister species, Embiotoca jacksoni and E. lateralis, are known to compete strongly for a preferred single food resource and may be used as a model of ecological interactions for the family. Along the California coast, the distribution of the two species differs. Embiotoca jacksoni has a continuous range, whereas E. lateralis shows a disjunction with a distribution gap in the Southern California Bight. Two hypotheses may explain this disjunct distribution. Ecological competition may have displaced E. lateralis in favor of E. jacksoni. Alternatively, a common vicariant event may have separated the species into northern and southern populations, followed by secondary contact in E. jacksoni but not in E. lateralis. The two hypotheses predict different phylogeographic and demographic signatures. Using a combined phylogeographic and coalescent approach based on mitochondrial control region data, we show that vicariance can only account for a portion of the observed divergences. Our results are compatible with a significant role played by ecological competition in the southern range of the species.