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2017
Pereira, RJ, Sasaki MC, Burton RS.  2017.  Adaptation to a latitudinal thermal gradient within a widespread copepod species: the contributions of genetic divergence and phenotypic plasticity. Proceedings of the Royal Society B-Biological Sciences. 284   10.1098/rspb.2017.0236   AbstractWebsite

Understanding how populations adapt to heterogeneous thermal regimes is essential for comprehending how latitudinal gradients in species diversification are formed, and how taxa will respond to ongoing climate change. Adaptation can occur by innate genetic factors, by phenotypic plasticity, or by a combination of both mechanisms. Yet, the relative contribution of such mechanisms to large-scale latitudinal gradients of thermal tolerance across conspecific populations remains unclear. We examine thermal performance in 11 populations of the intertidal copepod Tigriopus californicus, ranging from Baja California Sur (Mexico) to British Columbia (Canada). Common garden experiments show that survivorship to acute heat-stress differs between populations (by up to 3.8 degrees C in LD50 values), reflecting a strong genetic thermal adaptation. Using a split-brood experiment with two rearing temperatures, we also show that developmental phenotypic plasticity is beneficial to thermal tolerance (by up to 1.3 degrees C), and that this effect differs across populations. Although genetic divergence in heat tolerance strongly correlates with latitude and temperature, differences in the plastic response do not. In the context of climate warming, our results confirm the general prediction that low-latitude populations are most susceptible to local extinction because genetic adaptation has placed physiological limits closer to current environmental maxima, but our results also contradict the prediction that phenotypic plasticity is constrained at lower latitudes.

2016
Gleason, LU, Burton RS.  2016.  Regional patterns of thermal stress and constitutive gene expression in the marine snail Chlorostoma funebralis in northern and southern California. Marine Ecology Progress Series. 556:143-159.   10.3354/meps11850   AbstractWebsite

Southern California (USA) populations of the intertidal snail Chlorostoma funebralis occupy warmer climates than northern California populations, and southern populations are more thermally tolerant and have unique transcriptomic responses to heat stress compared to northern populations. To investigate how climate affects body temperature patterns for C. funebralis, iButton temperature loggers encased in empty C. funebralis shells (robosnails) were deployed at 3 northern and 3 southern California sites for 1.5 mo in the late summer and early fall of 2014, typically when maximum annual temperatures are reached. Measurements revealed that southern, thermally tolerant populations experienced higher average daily maximum and absolute maximum temperatures than northern, less tolerant populations, and that robosnails in southern, but not northern, California exceeded temperatures that cause 100% mortality. Similarly, the probability of a site reaching 27 degrees C, the temperature that induces the heat shock response in C. funebralis, was 3 times higher at the southern compared to the northern sites. To determine whether these exposures to stressful temperatures are related to gene expression differences, we then tested for a correlation between the probability of reaching 27 degrees C and the constitutive (non-induced) expression of genes previously implicated as pre-adapted in southern California populations. We identified 222 genes (including 14 involved in ubiquitin protein degradation, a response to heat stress) with a significant correlation. The results demonstrate how combining in situ temperature and transcriptome data can increase our understanding of thermal adaptation and better inform predictions regarding the impact of future climate change.

Gleason, LU, Burton RS.  2016.  Genomic evidence for ecological divergence against a background of population homogeneity in the marine snail Chlorostoma funebralis. Molecular Ecology. 25:3557-3573.   10.1111/mec.13703   AbstractWebsite

The balance between natural selection, gene flow and genetic drift is difficult to resolve in marine invertebrates with extensive dispersal and fluctuating population sizes. The intertidal snail Chlorostoma funebralis has planktonic larvae and previous work using mtDNA polymorphism reported no genetic population structure. Nevertheless, recent studies have documented differences in thermal tolerance and transcriptomic responses to heat stress between northern and southern California, USA, populations. To gain insight into the dynamics influencing adaptive divergence, we used double-digest restriction site-associated DNA (ddRAD) sequencing to identify 1861 genomewide, quality-filtered single-nucleotide polymorphism (SNP) loci for C.funebralis collected from three northern and three southern California sites (15 individuals per population). Considering all SNPs, there was no evidence for genetic differentiation among populations or regions (average F-ST=0.0042). However, outlier tests revealed 34 loci putatively under divergent selection between northern and southern populations, and structure and SNP tree analyses based on these outliers show clear genetic differentiation between geographic regions. Three of these outliers are known or hypothesized to be involved in stress granule formation, a response to environmental stress such as heat. Combined with previous work that found thermally tolerant southern populations show high baseline expression of stress response genes, these results further suggest that thermal stress is a strong selective pressure across C.funebralis populations. Overall, this study increases our understanding of the factors constraining local adaptation in marine organisms, while suggesting that ecologically driven, strong differentiation can occur at relevant loci in a species with planktonic larvae.

Stewart, JD, Beale CS, Fernando D, Sianipar AB, Burton RS, Semmens BX, Aburto-Oropeza O.  2016.  Spatial ecology and conservation of Manta birostris in the Indo-Pacific. Biological Conservation. 200:178-183.   10.1016/j.biocon.2016.05.016   AbstractWebsite

Information on the movements and population connectivity of the oceanic manta ray (Manta birostris) is scarce. The species has been anecdotally classified as a highly migratory species based on the pelagic habitats it often occupies, and migratory behavior exhibited by similar species. As a result, in the absence of ecological data, population declines in oceanic manta have been addressed primarily with international-scale management and conservation efforts. Using a combination of satellite telemetry, stable isotope and genetic analyses we demonstrate that, contrary to previous assumptions, the species appears to exhibit restricted movements and fine scale population structure. M. birostris tagged at four sites in the Indo-Pacific exhibited no long-range migratory movements and had non-overlapping geographic ranges. Using genetic and isotopic analysis, we demonstrate that the observed movements and population structure persist on multi-year and generational time scales. These data provide the first insights into the long-term movements and population structure of oceanic manta rays, and suggest that bottom-up, local or regional approaches to managing oceanic mantas could prove more effective than existing, international-scale management strategies. This case study highlights the importance of matching the scales at which management and relevant ecological processes occur to facilitate the effective conservation of threatened species. (C) 2016 Elsevier Ltd. All rights reserved.

Brandão, MC, Freire AS, Burton RS.  2016.  Estimating diversity of crabs (Decapoda: Brachyura) in a no-take marine protected area of the SW Atlantic coast through DNA barcoding of larvae. Systematics and Biodiversity. 14:288-302.: Taylor & Francis   10.1080/14772000.2016.1140245   Abstract

DNA barcoding was used to identify crab larvae from the Marine Biological Reserve of Arvoredo, encompassing a coastal archipelago off the SW Atlantic coast (27°S, 48°W). Partial mitochondrial COI or 16S rRNA gene sequences were obtained for 488 larvae, leading to the identification of 20 species. The COI sequences generated 13 barcode index numbers (BINs) within Barcode of Life Data Systems (BOLD), among which 11 were concordant with single species. DNA from ∼ 6% of the larvae did not amplify using the primers tested; based on external morphological characteristics, these larvae represented four possible additional operational taxonomic units (OTUs) at the family level. Intraspecific variation for the COI and 16S rRNA genes was found to be < 2.6% and < 2.1% respectively (Kimura 2-parameter distance), whereas interspecific divergence ranged from 7.9% to 21.5% and 6.4% to 14.5%, respectively. These results imply that both genes are suitable for use in species identification of brachyuran crabs of this area. Molecular identification of this group successfully enabled the diagnosis of larvae of closely related species, including congeners in Mithrax, Achelous and Callinectes. In addition, eight out of 20 species recognized represent new records for the reserve suggesting that the brachyuran fauna in the area has been underestimated based on traditional biodiversity measures. The availability of primers suited to the targeted species, and the development of a taxonomically comprehensive DNA barcoding database are the major recommendations to improve the accuracy and feasibility of using DNA barcoding for species identification of SW Atlantic brachyuran crabs.

Pereira, RJ, Barreto FS, Pierce NT, Carneiro M, Burton RS.  2016.  Transcriptome-wide patterns of divergence during allopatric evolution. Molecular Ecology. 25:1478-1493.   10.1111/mec.13579   AbstractWebsite

Recent studies have revealed repeated patterns of genomic divergence associated with species formation. Such patterns suggest that natural selection tends to target a set of available genes, but is also indicative that closely related taxa share evolutionary constraints that limit genetic variability. Studying patterns of genomic divergence among populations within the same species may shed light on the underlying evolutionary processes. Here, we examine transcriptome-wide divergence and polymorphism in the marine copepod Tigriopus californicus, a species where allopatric evolution has led to replicate sets of populations with varying degrees of divergence and hybrid incompatibility. Our analyses suggest that relatively small effective population sizes have resulted in an exponential decline of shared polymorphisms during population divergence and also facilitated the fixation of slightly deleterious mutations within allopatric populations. Five interpopulation comparisons at three different stages of divergence show that nonsynonymous mutations tend to accumulate in a specific set of proteins. These include proteins with central roles in cellular metabolism, such as those encoded in mtDNA, but also include an additional set of proteins that repeatedly show signatures of positive selection during allopatric divergence. Although our results are consistent with a contribution of nonadaptive processes, such as genetic drift and gene expression levels, generating repeatable patterns of genomic divergence in closely related taxa, they also indicate that adaptive evolution targeting a specific set of genes contributes to this pattern. Our results yield insights into the predictability of evolution at the gene level. See also the Perspective by Renaut and Dion-Cote

Bonin, CA, Goebel ME, O'Corry-Crowe GM, Burton RS.  2016.  Impacts of ecology and behavior on Antarctic fur seal remating and relatedness. Journal of Experimental Marine Biology and Ecology. 476:72-77.   10.1016/j.jembe.2015.12.008   AbstractWebsite

Antarctic fur seals (Arctocephalus gazella) are polygynous and both sexes are typically faithful to a breeding site. These characteristics could promote remating among individuals over time, leading to increased relatedness levels and negatively affecting genetic diversity. To examine this issue, the reproductive output of 55 females was monitored annually for 12 years and their pups were sampled (n = 280) and genotyped using 17 microsatellite markers. A full likelihood pedigree inference method was used to confirm maternities inferred in the field and estimate the number of full sibling pups born across years. Relatedness coefficients were estimated for pairs of individuals in the pedigree and compared to simulated values for each relationship category. There were nine cases where a female mated with the same male twice and one case where a female mated with the same male three times over the study period. The observed relatedness coefficients estimated among the sampled pups matched the simulated distribution for half-siblings. In addition, no first order relatives were found among the fur seal mothers studied, nor did observed relatedness coefficient distributions differ significantly from simulated values. Together, these results suggest a low remating rate and a negligible effect of remating on pair-wise relatedness. Territorial male replacement over time as well as female small-scale movements, driven by suitable pupping habitat, likely contribute to the low remating frequency observed in Antarctic fur seals. (C) 2015 Elsevier B.V. All rights reserved.

2015
Harada, AE, Lindgren EA, Hermsmeier MC, Rogowski PA, Terrill E, Burton RS.  2015.  Monitoring spawning activity in a Southern California marine protected area using molecular identification of fish eggs. Plos One. 10   10.1371/journal.pone.0134647   AbstractWebsite

In order to protect the diverse ecosystems of coastal California, a series of marine protected areas (MPAs) have been established. The ability of these MPAs to preserve and potentially enhance marine resources can only be assessed if these habitats are monitored through time. This study establishes a baseline for monitoring the spawning activity of fish in the MPAs adjacent to Scripps Institution of Oceanography (La Jolla, CA, USA) by sampling fish eggs from the plankton. Using vertical plankton net tows, 266 collections were made from the Scripps Pier between 23 August 2012 and 28 August 2014; a total of 21,269 eggs were obtained. Eggs were identified using DNA barcoding: the COI or 16S rRNA gene was amplified from individual eggs and sequenced. All eggs that were successfully sequenced could be identified from a database of molecular barcodes of California fish species, resulting in species-level identification of 13,249 eggs. Additionally, a surface transport model of coastal circulation driven by current maps from high frequency radar was used to construct probability maps that estimate spawning locations that gave rise to the collected eggs. These maps indicated that currents usually come from the north but water parcels tend to be retained within the MPA; eggs sampled at the Scripps Pier have a high probability of having been spawned within the MPA. The surface transport model also suggests that although larvae have a high probability of being retained within the MPA, there is also significant spill-over into nearby areas outside the MPA. This study provides an important baseline for addressing the extent to which spawning patterns of coastal California species may be affected by future changes in the ocean environment.

Barreto, FS, Schoville SD, Burton RS.  2015.  Reverse genetics in the tide pool: knock-down of target gene expression via RNA interference in the copepod Tigriopus californicus. Molecular Ecology Resources. 15:868-879.   10.1111/1755-0998.12359   AbstractWebsite

Reverse genetic tools are essential for characterizing phenotypes of novel genes and testing functional hypotheses generated from next-generation sequencing studies. RNA interference (RNAi) has been a widely used technique for describing or quantifying physiological, developmental or behavioural roles of target genes by suppressing their expression. The marine intertidal copepod Tigriopus californicus has become an emerging model for evolutionary and physiological studies, but this species is not amenable to most genetic manipulation approaches. As crustaceans are susceptible to RNAi-mediated gene knock-down, we developed a simple method for delivery of gene-specific double-stranded RNA that results in significant suppression of target gene transcription levels. The protocol was examined on five genes of interest, and for each, at least 50% knock-down in expression was achieved. While knock-down levels did not reach 100% in any trial, a well-controlled experiment with one heat-shock gene showed unambiguously that such partial gene suppression may cause dramatic changes in phenotype. Copepods with suppressed expression of heat-shock protein beta 1 (hspb1) exhibited dramatically decreased tolerance to high temperatures, validating the importance of this gene during thermal stress, as proposed by a previous study. The application of this RNAi protocol in T.californicus will be invaluable for examining the role of genes putatively involved in reproductive isolation, mitochondrial function and local adaptation.

Barreto, FS, Pereira RJ, Burton RS.  2015.  Hybrid dysfunction and physiological compensation in gene expression. Molecular Biology and Evolution. 32:613-622.   10.1093/molbev/msu321   AbstractWebsite

The formation of new species is often a consequence of genetic incompatibilities accumulated between populations during allopatric divergence. When divergent taxa interbreed, these incompatibilities impact physiology and have a direct cost resulting in reduced hybrid fitness. Recent surveys of gene regulation in interspecific hybrids have revealed anomalous expression across large proportions of the genome, with 30-70% of all genes exhibiting transgressive expression (i.e., higher or lower levels compared with both parental taxa), and these were mostly in the direction of downregulation. However, as most of these studies have focused on pairs of species exhibiting high degrees of reproductive isolation, the association between regulatory disruption and reduced hybrid fitness prior to species formation remains unclear. Within the copepod species Tigriopus californicus, interpopulation hybrids at F-2 or later generations show reduced fitness associated with mitochondrial dysfunction. Here we show that in contrast to studies of interspecific hybrids, only 1.2% of the transcriptome is transgressively expressed in F3+ interpopulation hybrids of T. californicus, and nearly 80% of these genes are overexpressed rather than underexpressed; remarkably, none of these genes are among those showing divergent expression between parentals, nor is magnitude of transgressive gene expression in hybrids dependent on levels of protein sequence divergence. Moreover, many genes with transgressive expression are components of functional pathways impacted by mitonuclear incompatibilities in hybrid T. californicus (e.g., oxidative phosphorylation and antioxidant response). Our results suggest that hybrid breakdown at early stages of speciation may result from initial incompatibilities amplified by the cost of compensatory physiological responses.

Gleason, LU, Burton RS.  2015.  RNA-seq reveals regional differences in transcriptome response to heat stress in the marine snail Chlorostoma funebralis. Molecular Ecology. 24:610-627.   10.1111/mec.13047   AbstractWebsite

To investigate the role of gene expression in adaptation of marine ectotherms to different temperatures, we examined the transcriptome-wide thermal stress response in geographically separated populations of the intertidal snail Chlorostoma funebralis. Snails from two southern (heat tolerant) and two northern (heat sensitive) populations were acclimated to a common thermal environment, exposed to an environmentally relevant thermal stress and analysed using RNA-seq. Pooling across all populations revealed 306 genes with differential expression between control and heat-stressed samples, including 163 significantly upregulated and 143 significantly downregulated genes. When considered separately, regional differences in response were widely apparent. Heat shock proteins (Hsps) were upregulated in both regions, but the magnitude of response was significantly greater in northern populations for most Hsp70s, while the southern populations showed greater upregulation for approximately half of the Hsp40s. Of 177 stress-responsive genes in northern populations, 55 responded to heat stress only in northern populations. Several molecular chaperones and antioxidant genes that were not differentially expressed in southern populations showed higher expression under control conditions compared with northern populations. This suggests that evolution of elevated expression of these genes under benign conditions preadapts the southern populations to frequent heat stress and contributes to their higher thermal tolerance. These results indicate that evolution has resulted in different transcriptome responses across populations, including upregulation of genes in response to stress and preadaptation of genes in anticipation of stress (based on evolutionary history of frequent heat exposure). The relative importance of the two mechanisms differs among gene families and among populations.

2014
Tangwancharoen, S, Burton RS.  2014.  Early life stages are not always the most sensitive: heat stress responses in the copepod Tigriopus californicus. Marine Ecology Progress Series. 517:75-83.   10.3354/meps11013   AbstractWebsite

Because of their complex life histories, different life stages of many marine invertebrates may be exposed to varying environmental challenges. Ultimately, the life stage that is least tolerant of its environment will determine the species' abundance and distribution. The intertidal copepod Tigriopus californicus lives in high intertidal pools along the Pacific coast of North America. Unlike most other invertebrates, the different life stages of T. californicus all share the same tidepool habitat. To determine physiological tolerances of various life history stages of this species, we examined responses to acute heat stress in nauplii, copepodids, and adults from 6 populations along a latitudinal gradient. Results show that early developmental stages (nauplii and cope podids) are generally more tolerant than adults. Our results contrast with the widely accepted generalization that larval forms are more sensitive to physical stressors than adults. As previously observed in adults, nauplii and copepodids from southern populations survive higher temperatures than those from northern populations. Acute heat stress was found to delay development but did not affect adult size. We hypothesize that variation in the thermal tolerance of early life stages among intertidal species reflects ecological differences in larval habitats: where larvae remain in the intertidal zone and experience the same high temperatures as adults, selection will favor high larval thermal tolerance, while in species with planktonic larvae, the buffered temperature regime of the water column might relax such selection, and thermal tolerance will be highest in the more exposed intertidal adults.

Bonin, CA, Goebel ME, Hoffman JI, Burton RS.  2014.  High male reproductive success in a low-density Antarctic fur seal (Arctocephalus gazella) breeding colony. Behavioral Ecology and Sociobiology. 68:597-604.   10.1007/s00265-013-1674-7   AbstractWebsite

Understanding how population density influences mating systems may lead to important insights into the plasticity of breeding behavior, but few natural systems allow for such studies. Antarctic fur seals (Arctocephalus gazella) provide an interesting model system because they breed in colonies of varying densities. Previous studies have largely focused on a high-density site at Bird Island, South Georgia. Here, 13 highly polymorphic microsatellite loci were used to conduct a genetic analysis of a low-density breeding colony of this species at Livingston Island, approximately 1,600 km south of South Georgia. The majority of adults seen ashore (n = 54) were sampled together with every pup born (n = 97) over four consecutive years. Paternities were confidently assigned for 34 out of the 97 pups. Two out of 23 sampled males accounted for the paternity of 28 % of all pups sampled during the study and 82 % of the pups with an assigned father. Moreover, a full likelihood pedigree inference method assigned a further eight paternities to a single unsampled male seal that is inferred to have held a territory during the season before the study began. The most successful males in our study easily surpassed the previous record for the total number of pups sired per male seal for the species. Furthermore, we identified two triads of full siblings implying that their parents remated in three consecutive years. These findings suggest that territorial male fur seals may achieve greater success in monopolizing access to breeding females when population density is relatively low.

Fisch, KM, Mahardja B, Burton RS, May B.  2014.  Hybridization between delta smelt and two other species within the family Osmeridae in the San Francisco Bay-Delta. Conservation Genetics. 15:489-494.   10.1007/s10592-013-0555-y   AbstractWebsite

Hybridization among closely related species may pose a threat to species persistence, especially between native and introduced species. We analyzed nine microsatellite loci, mitochondrial sequences and 16 species-specific single nucleotide polymorphisms (SNPs) in two native species (delta smelt and longfin smelt) and one introduced species (wakasagi smelt) in the family Osmeridae to describe the extent of hybridization among these species in the San Francisco Bay-Delta, CA, USA. We identified 29 putative hybrids with a microsatellite-based Bayesian assignment method, and we further screened these putative hybrids with the SNP loci and mitochondrial DNA (mtDNA) sequencing. From the Yolo Bypass, 11 % of morphologically ambiguous individuals were F-1 hybrids and 0.1 % of positively identified delta smelt from throughout the San Francisco Bay-Delta were F-1 hybrids according to their SNP genotypes. mtDNA sequencing revealed wakasagi smelt as the maternal parent for all five delta smelt x wakasagi smelt hybrids and longfin smelt as the maternal parent for the single longfin smelt 9 delta smelt hybrid. Hybridization among these three species appears to occur at relatively low frequencies and may not be an immediate threat to the persistence of the imperiled native species; however, the presence of hybrid individuals warrants continued monitoring.

Pereira, RJ, Barreto FS, Burton RS.  2014.  Ecological novelty by hybridization: Experimental evidence for increased thermal tolerance by transgressive segregation in tigriopus californicus. Evolution. 68:204-215.   10.1111/evo.12254   AbstractWebsite

Early generations of hybrids can express both genetic incompatibilities and phenotypic novelty. Insights into whether these conflicting interactions between intrinsic and extrinsic selection persist after a few generations of recombination require experimental studies. To address this question, we use interpopulation crosses and recombinant inbred lines (RILs) of the copepod Tigriopus californicus, and focus on two traits that are relevant for the diversification of this species: survivorship during development and tolerance to thermal stress. Experimental crosses between two population pairs show that most RILs between two heat-tolerant populations show enhanced tolerance to temperatures that are lethal to the respective parentals, whereas RILs between a heat-tolerant and a heat-sensitive population are intermediate. Although interpopulation crosses are affected by intrinsic selection at early generational hybrids, most of the sampled F-9 RILs have recovered fitness to the level of their parentals. Together, these results suggest that a few generations of recombination allows for an independent segregation of the genes underlying thermal tolerance and cytonuclear incompatibilities, permitting certain recombinant lineages to survive in niches previously unused by parental taxa (i.e., warmer thermal environments) without incurring intrinsic selection.

2013
Fisch, KM, Ivy JA, Burton RS, May B.  2013.  Evaluating the Performance of Captive Breeding Techniques for Conservation Hatcheries: A Case Study of the Delta Smelt Captive Breeding Program. Journal of Heredity. 104:92-104.   10.1093/jhered/ess084   AbstractWebsite

The delta smelt, an endangered fish species endemic to the San Francisco Bay-Delta, California, United States, was recently brought into captivity for species preservation. This study retrospectively evaluates the implementation of a genetic management plan for the captive delta smelt population. The captive genetic management plan entails tagging fish, molecular data collection, pedigree reconstruction, relatedness estimation, and recommending fish crosses annually in an effort to minimize the average coancestry in the population and limit inbreeding. We employed 12 microsatellite DNA markers to examine temporal genetic diversity in consecutive, discrete generations to determine the effects of intensive genetic management on the population and to quantify the amount of wild genetic diversity present within each captive generation. Wild fish are incorporated into the captive population each generation to minimize genetic drift, and 91% of the original founders are still represented in the F-3 generation. The average mean kinship in the third generation in captivity was 0.0035. There was no evidence of significant genetic divergence of the captive population from the wild population. The results of this study yield management insights into the practical application of genetic management plans for captive populations and conservation hatcheries, in an attempt to preserve the genetic integrity of endangered species.

Barreto, FS, Burton RS.  2013.  Evidence for Compensatory Evolution of Ribosomal Proteins in Response to Rapid Divergence of Mitochondrial rRNA. Molecular Biology and Evolution. 30:310-314.   10.1093/molbev/mss228   AbstractWebsite

Rapid evolution of mitochondrial DNA (mtDNA) places intrinsic selective pressures on many nuclear genes involved in mitochondrial functions. Mitochondrial ribosomes, for example, are composed of mtDNA-encoded ribosomal RNAs (rRNAs) and a set of more than 60 nuclear-encoded ribosomal proteins (mRP) distinct from the cytosolic RPs (cRP). We hypothesized that the rapid divergence of mt-rRNA would result in rapid evolution of mRPs relative to cRPs, which respond to slowly evolving nuclear-encoded rRNA. In comparisons of rates of nonsynonymous and synonymous substitutions between a pair of divergent populations of the copepod Tigriopus californicus, we found that mRPs showed elevated levels of amino acid changes relative to cRPs. This pattern was equally strong at the interspecific level, between three pairs of sister species (Nasonia vitripennis vs. N. longicornis, Drosophila melanogaster vs. D. simulans, and Saccharomyces cerevisae vs. S. paradoxus). This high rate of mRP evolution may result in intergenomic incompatibilities between taxonomic lineages, and such incompatibilities could lead to dysfunction of mitochondrial ribosomes and the loss of fitness observed among interpopulation hybrids in T. californicus and interspecific hybrids in other species.

Nosal, AP, Lewallen EA, Burton RS.  2013.  Multiple paternity in leopard shark (Triakis semifasciata) litters sampled from a predominantly female aggregation in La Jolla, California, USA. Journal of Experimental Marine Biology and Ecology. 446:110-114.   10.1016/j.jembe.2013.05.002   AbstractWebsite

The number of sires per litter was determined for the leopard shark (Triakidae: Triakis semifasciata) to investigate the potential effect of female-biased aggregation behavior on the frequency of multiple paternity (F-MP). Four highly polymorphic microsatellite markers were developed and used to genotype 449 pups from 22 litters (20.4 +/- 7.0 pups per litter) sampled from pregnant females collected from a female-dominated leopard shark aggregation in La Jolla, California, USA. Multiple paternity was detected in 8 of 22 litters (F-MP = 36.4%), each having two sires per litter. The relatively low F-MP (compared to other shark species) is generally consistent with the hypothesis that female aggregation behavior reduces mating attempts by males and thus limits genetic polyandry. Significant interannual variability in F-MP observed between two years of the study (2010: F-MP = 20.0%, n = 10, and 2011: F-MP = 83.3%, n = 6) appears to be correlated with the frequency of males in the aggregation. Although females may benefit indirectly from mating with multiple males by promoting sperm competition and hedging against nonviable sperm, the most probable explanation for genetic polyandry in the leopard shark appears to be "convenience polyandry," where females acquiesce to superfluous mating attempts if the costs of resistance outweigh the costs of capitulation. Thus, F-MP is expected to increase as the male-to-female ratio increases and as capacity of females to resist coercive males decreases at the time and place of mating. (C) 2013 Elsevier B.V. All rights reserved.

Barreto, FS, Burton RS.  2013.  Elevated oxidative damage is correlated with reduced fitness in interpopulation hybrids of a marine copepod. Proceedings of the Royal Society B-Biological Sciences. 280   10.1098/rspb.2013.1521   AbstractWebsite

Aerobic energy production occurs via the oxidative phosphorylation pathway (OXPHOS), which is critically dependent on interactions between the 13 mitochondrial DNA (mtDNA)-encoded and approximately 70 nuclear-encoded protein subunits. Disruptive mutations in any component of OXPHOS can result in impaired ATP production and exacerbated oxidative stress; in mammalian systems, such mutations are associated with ageing as well as numerous diseases. Recent studies have suggested that oxidative stress plays a role in fitness trade-offs in life-history evolution and functional ecology. Here, we show that outcrossing between populations with divergent mtDNA can exacerbate cellular oxidative stress in hybrid offspring. In the copepod Tigriopus californicus, we found that hybrids that showed evidence of fitness breakdown (low fecundity) also exhibited elevated levels of oxidative damage to DNA, whereas those with no clear breakdown did not show significantly elevated damage. The extent of oxidative stress in hybrids appears to be dependent on the degree of genetic divergence between their respective parental populations, but this pattern requires further testing using multiple crosses at different levels of divergence. Given previous evidence in T. californicus that hybridization disrupts nuclear/mitochondrial interactions and reduces hybrid fitness, our results suggest that such negative intergenomic epistasis may also increase the production of damaging cellular oxidants; consequently, mtDNA evolution may play a significant role in generating postzygotic isolating barriers among diverging populations.

Gleason, LU, Burton RS.  2013.  Phenotypic evidence for local adaptation to heat stress in the marine snail Chlorostoma (formerly Tegula) funebralis. Journal of Experimental Marine Biology and Ecology. 448:360-366.   10.1016/j.jembe.2013.08.008   AbstractWebsite

Southern California (USA) populations of the intertidal marine snail Chlorostoma (formerly Tegula) funebralis generally occupy warmer climates and are exposed to high air temperatures during low tides more often than northern California populations. Available genetic data suggest there is extensive gene flow across a broad range of C funebralis populations, so it is unclear if populations can adapt to differences in local environments. To test for population-specific responses to heat stress, three phenotypic assays were performed on three northern and on three southern populations of C. funebralis, after acclimation to common-garden conditions in the laboratory. Thermal drop-down, heat stress mortality, and heat stress reattachment assays were designed to evaluate ecologically relevant phenotypic responses to heat stress; these assays assessed tolerance during, mortality following, and speed of recovery following heat stress. The latter two tests indicate that southern populations consistently suffer significantly lower mortality and recover significantly more quickly following heat stress compared to northern populations. Hierarchical cluster analysis of stress response data clearly identified northern California and southern California regional groupings of populations. Thus, these results indicate that southern populations have higher tolerance to heat stress than northern populations and suggest that adaptation to local environmental differences can evolve despite moderate potential for larval dispersal in this species. Accounting for intraspecific population variation in thermal tolerance may provide important insights for predicting how species distributions will respond to global warming. (C) 2013 Elsevier B.V. All rights reserved.

Bonin, CA, Goebel ME, Forcada J, Burton RS, Hoffman JI.  2013.  Unexpected genetic differentiation between recently recolonized populations of a long-lived and highly vagile marine mammal. Ecology and Evolution. 3:3701-3712.   10.1002/ece3.732   AbstractWebsite

Many species have been heavily exploited by man leading to local extirpations, yet few studies have attempted to unravel subsequent recolonization histories. This has led to a significant gap in our knowledge of the long-term effects of exploitation on the amount and structure of contemporary genetic variation, with important implications for conservation. The Antarctic fur seal provides an interesting case in point, having been virtually exterminated in the nineteenth century but subsequently staged a dramatic recovery to recolonize much of its original range. Consequently, we evaluated the hypothesis that South Georgia (SG), where a few million seals currently breed, was the main source of immigrants to other locations including Livingston Island (LI), by genotyping 366 individuals from these two populations at 17 microsatellite loci and sequencing a 263bp fragment of the mitochondrial hypervariable region 1. Contrary to expectations, we found highly significant genetic differences at both types of marker, with 51% of LI individuals carrying haplotypes that were not observed in 246 animals from SG. Moreover, the youngest of three sequentially founded colonies at LI showed greater similarity to SG at mitochondrial DNA than microsatellites, implying temporal and sex-specific variation in recolonization. Our findings emphasize the importance of relict populations and provide insights into the mechanisms by which severely depleted populations can recover while maintaining surprisingly high levels of genetic diversity.

Burton, RS, Pereira RJ, Barreto FS.  2013.   Cytonuclear genomic interactions and hybrid breakdown. Annual Reviews of Ecology, Evolution and Systematics. 44:281-302.   10.1146/annurev-ecolsys-110512-135758  
2012
Schoville, SD, Barreto FS, Moy GW, Wolff A, Burton RS.  2012.  Investigating the molecular basis of local adaptation to thermal stress: population differences in gene expression across the transcriptome of the copepod Tigriopus californicus. BMC Evolutionary Biology. 12   10.1186/1471-2148-12-170   AbstractWebsite

Background: Geographic variation in the thermal environment impacts a broad range of biochemical and physiological processes and can be a major selective force leading to local population adaptation. In the intertidal copepod Tigriopus californicus, populations along the coast of California show differences in thermal tolerance that are consistent with adaptation, i.e., southern populations withstand thermal stresses that are lethal to northern populations. To understand the genetic basis of these physiological differences, we use an RNA-seq approach to compare genome-wide patterns of gene expression in two populations known to differ in thermal tolerance. Results: Observed differences in gene expression between the southern (San Diego) and the northern (Santa Cruz) populations included both the number of affected loci as well as the identity of these loci. However, the most pronounced differences concerned the amplitude of up-regulation of genes producing heat shock proteins (Hsps) and genes involved in ubiquitination and proteolysis. Among the hsp genes, orthologous pairs show markedly different thermal responses as the amplitude of hsp response was greatly elevated in the San Diego population, most notably in members of the hsp70 gene family. There was no evidence of accelerated evolution at the sequence level for hsp genes. Among other sets of genes, cuticle genes were up-regulated in SD but down-regulated in SC, and mitochondrial genes were down-regulated in both populations. Conclusions: Marked changes in gene expression were observed in response to acute sub-lethal thermal stress in the copepod T. californicus. Although some qualitative differences were observed between populations, the most pronounced differences involved the magnitude of induction of numerous hsp and ubiquitin genes. These differences in gene expression suggest that evolutionary divergence in the regulatory pathway(s) involved in acute temperature stress may offer at least a partial explanation of population differences in thermal tolerance observed in Tigriopus.

Burton, RS, Barreto FS.  2012.  A disproportionate role for mtDNA in Dobzhansky-Muller incompatibilities? Molecular Ecology. 21:4942-4957.   10.1111/mec.12006   AbstractWebsite

Evolution in allopatric populations can lead to incompatibilities that result in reduced hybrid fitness and ultimately reproductive isolation upon secondary contact. The DobzhanskyMuller (DM) model nicely accounts for the evolution of such incompatibilities. Although DM incompatibilities were originally conceived as resulting of interactions between nuclear genes, recent studies have documented cases where incompatibilities have arisen between nuclear and mitochondrial genomes (mtDNA). Although mtDNA comprises only a tiny component (typically << 0.01%) of an organism's genetic material, several features of mtDNA may lead to a disproportionate contribution to the evolution of hybrid incompatibilities: (i) essentially all functions of mtDNA require interaction with nuclear gene products. All mtDNA-encoded proteins are components of the oxidative phosphorylation (OXPHOS) system and all mtDNA-encoded RNAs are part of the mitochondrial protein synthetic machinery; both processes require interaction with nuclear-encoded proteins for function. (ii) Transcription and replication of mtDNA also involve mitonuclear interactions as nuclear-encoded proteins must bind to regulatory motifs in the mtDNA to initiate these processes. (iii) Although features of mtDNA vary amongst taxa, metazoan mtDNA is typically characterized by high nucleotide substitution rates, lack of recombination and reduced effective population sizes that collectively lead to increased chance fixation of mildly deleterious mutations. Combined, these features create an evolutionary dynamic where rapid mtDNA evolution favours compensatory nuclear gene evolution, ultimately leading to co-adaptation of mitochondrial and nuclear genomes. When previously isolated lineages hybridize in nature or in the lab, intergenomic co-adaptation is disrupted and hybrid breakdown is observed; the role of intergenomic co-adaptation in hybrid breakdown and speciation will generally be most pronounced when rates of mtDNA evolution are high or when restricted gene flow results in significant population differentiation.

Benham, CE, Supernault KJ, Burton RS.  2012.  Genetic assessment of the population connectivity of the red urchin (Strongylocentrotus franciscanus). Journal of Experimental Marine Biology and Ecology. 432:47-54.   10.1016/j.jembe.2012.07.011   AbstractWebsite

A set of five microsatellite genetic markers was used to examine connectivity among populations of the red urchin, Strongylocentrotus franciscanus, collected from five locations in California and two locations in British Columbia, Canada. Consistent with previous studies, there was little evidence of differentiation among the California populations. However, significant divergence (F-ST=0.039), as well as isolation by distance (IBD) (R-2=0.2815, p=0.024), was observed between the California and British Columbia populations. These results show for the first time that, on a range wide scale, populations of red urchins are genetically divergent. Although the detected differentiation is low, it suggests that even the estimated 7-19 month planktonic larval duration of this species fails to homogenize the gene pool across the species range. (C) 2012 Elsevier B.V. All rights reserved.