Patterns of Genomic Divergence and Signals of Selection in Sympatric and Allopatric Northeastern Pacific and Sea of Cortez Populations of the Sargo (Anisotremus davidsonii) and Longjaw Mudsucker (Gillichthys mirabilis)

Studying how isolation can impact population divergence and adaptation in co-distributed species can bring us closer to understanding how landscapes affect biodiversity. The Sargo, Anisotremus davidsonii (Haemulidae), and the Longjaw mudsucker, Gillichthys mirabilis (Gobiidae), offer a notable framework to study such mechanisms as their Pacific populations cross phylogeographic breaks at Point Conception, California, United States, and Punta Eugenia, Mexico, and are separated to those in the Sea of Cortez by the Baja California peninsula. Here, thousands of loci are genotyped from 48 Sargos and 73 mudsuckers using RADseq to characterize overall genomic divergence, and search for common patterns of putatively neutral and non-neutral structure based on outlier loci among populations with hypothesized different levels of isolation. We further search for parallels between population divergence and the total proportion of outliers, outlier FST distribution, and the proportion of outliers matching coding regions in GenBank. Statistically significant differentiation is seen across Point Conception in mudsucker (FST = 0.15), Punta Eugenia in Sargo (FST = 0.02), and on either side of the Baja California peninsula in both species (FST = 0.11 and 0.23, in Sargo and mudsucker, respectively). Each species shows structure using neutral and non-neutral loci. Finally, higher population divergence yields a more even distribution of outliers along their differentiation range but does not always translate into higher outlier proportions or higher rates in which outliers are matched to coding regions. If repeated in similar systems, observed genomic patterns might reveal speciation signatures in diverse networks of population isolation.

Effects of thermal acclimation on transcriptional responses to acute heat stress in the eurythermal fish Gillichthys mirabilis (Cooper)

The capacities of eurythermal ectotherms to withstand wide ranges of temperature are based, in part, on abilities to modulate gene expression as body temperature changes, notably genes encoding proteins of the cellular stress response. Here, using a complementary DNA microarray, we investigated the sequence in which cellular stress response-linked genes are expressed during acute heat stress, to elucidate how severity of stress affects the categories of genes changing expression. We also studied how prior acclimation history affected gene expression in response to acute heat stress. Eurythermal goby fish ( Gillichthys mirabilis ) were acclimated to 9 ± 0.5, 19 ± 0.5, and 28 ± 0.5°C for 1 mo. Then fish were given an acute heat ramp (4°C/h), and gill tissues were sampled every +4°C to monitor gene expression. The average onset temperature for a significant change in expression during acute stress increased by ∼2°C for each ∼10°C increase in acclimation temperature. For some genes, warm acclimation appeared to obviate the need for expression change until the most extreme temperatures were reached. Sequential expression of different categories of genes reflected severity of stress. Regardless of acclimation temperature, the gene encoding heat shock protein 70 ( HSP70) was upregulated strongly during mild stress; the gene encoding the proteolytic protein ubiquitin ( UBIQ) was upregulated at slightly higher temperatures; and a gene encoding a protein involved in cell cycle arrest and apoptosis, cyclin-dependent kinase inhibitor 1B ( CDKN1B), was upregulated only under extreme stress. The tiered, stress level-related expression patterns and the effects of acclimation on induction temperature yield new insights into the fundamental mechanisms of eurythermy.

Transcriptional responses to thermal acclimation in the eurythermal fish Gillichthys mirabilis (Cooper 1864)

Thermal acclimation (acclimatization) capacity may be critical for determining how successfully an ectotherm can respond to temperature change, and adaptive shifts in gene expression may be pivotal for mediating these acclimatory responses. Using a cDNA microarray, we examined transcriptional profiles in gill tissue of a highly eurythermal goby fish, Gillichthys mirabilis , following 4 wk of acclimation to 9°C, 19°C, or 28°C. Overall, gill transcriptomes were not strikingly different among acclimation groups. Of the 1,607 unique annotated genes on the array, only 150 of these genes (9%) were significantly different in expression among the three acclimation groups (ANOVA, false discovery rate < 0.05). Principal component analysis revealed that 59% of the variation in expression among these genes was described by an expression profile that is upregulated with increasing acclimation temperature. Gene ontology analysis of these genes identified protein biosynthesis, transport, and several metabolic categories as processes showing the greatest change in expression. Our results suggest that energetic costs of macromolecular turnover and membrane-localized transport rise with acclimation temperature. The upregulation of several classes of stress-related proteins, e.g., heat shock proteins, seen in the species' response to acute thermal stress was not observed in the long-term 28°C-acclimated fish. The transcriptional differences found among the acclimation groups thus may reflect an acclimation process that has largely remedied the effects of acute thermal stress and established a new steady-state condition involving changes in relative energy costs for different processes. This pattern of transcriptional alteration in steady-state acclimated fish may be a signature of eurythermy.