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Garza, J. C.

Publications and source records attributed to Garza, J. C..

9 recordsLinked to original sources

The genetic architecture of ecotypic differentiation in Chinook salmon of the California Central Valley

Understanding the genomic details underlying complex behavioral traits is a foundational pursuit in biology. We use genomic and genetic techniques to dissect the heritable underpinnings of adult migration timing of Chinook salmon in the California Central Valley (CCV), home to several ecotypes not found elsewhere. We find that a previously described genomic region contributes to the seasonal shift in adult freshwater migration in the CCV, as in other river basins, but we further identify two functional domains in this locus that separately and additively influence the trait, with each allele copy affecting timing by [~]two weeks. We show how the evolution of a unique ecotype in the CCV is partially due to an allele derived from the more widespread early-migrating haplotype. However, the genomic background of the evolutionarily differentiated ecotypes contributes a similar amount to trait variation. We show how a relatively simple five-allele genetic system, in concert with genomic backgrounds, can create a remarkable diversity of phenotypes and ecotypes for this iconic species. TeaserA diverse complex of salmon ecotypes is explained by a simple two-locus system and evolutionarily derived genomic backgrounds.

genetics↗

Recent adaptation in an imperiled salmonid revealed by museum genomics

Steelhead/rainbow trout (Oncorhynchus mykiss) is an imperiled salmonid with two main life history strategies: migrate to the ocean or remain in freshwater. Domesticated hatchery forms of this species have been stocked into almost all California waterbodies, possibly resulting in introgression into natural populations and altered population structure. We compared whole-genome sequence data from contemporary populations against a set of museum population samples of steelhead from the same locations that were collected prior to most hatchery stocking. We observed minimal introgression and few steelhead-hatchery trout hybrids despite a century of extensive stocking. Our historical data show signals of introgression with a sister species and indications of an early hatchery facility. Finally, we found that migration-associated haplotypes have become less frequent over time, a likely adaptation to decreased opportunities for migration. Since contemporary migration-associated haplotype frequencies have been used to guide species management, we consider this to be a rare example of shifting baseline syndrome that has been validated with historical data. We suggest cautious optimism that a century of hatchery stocking has had minimal impact on California steelhead population genetic structure, but we note that continued shifts in life history may lead to further declines in the ocean-going form of the species.

genomics↗

Heterogeneous genetic basis of age at maturity in salmonid fishes

Understanding the genetic basis of repeated evolution of the same phenotype across taxa is a fundamental aim in evolutionary biology and has applications to conservation and management. However, the extent to which interspecific life-history trait polymorphisms share evolutionary pathways remains under-explored. We address this gap by studying the genetic basis of a key life-history trait, age at maturity, in four species of Pacific salmon (genus Oncorhynchus) that exhibit intra- and interspecific variation in this trait - Chinook Salmon, Coho Salmon, Sockeye Salmon, and Steelhead Trout. We tested for associations in all four species between age at maturity and two genome regions, six6 and vgll3, that are strongly associated with the same trait in Atlantic Salmon (Salmo salar). We also conducted a genome-wide association analysis in Steelhead to assess whether additional regions were associated with this trait. We found the genetic basis of age at maturity to be heterogeneous across salmonid species. Significant associations between six6 and age at maturity were observed in two of the four species, Sockeye and Steelhead, with the association in Steelhead being particularly strong in both sexes (p = 4.46x10-9 after adjusting for genomic inflation). However, no significant associations were detected between age at maturity and the vgll3 genome region in any of the species, despite its strong association with the same trait in Atlantic Salmon. We discuss possible explanations for the heterogeneous nature of the genetic architecture of this key life-history trait, as well as the implications of our findings for conservation and management.

evolutionary biology↗

Ankyrin-G-190 palmitoylation mediates dendrite and spine morphogenesis and is altered in response to lithium

AnkG, encoded by the ANK3 gene, is a multifunctional scaffold protein with complex isoform expression: the 480 kDa and 270 kDa isoforms have roles at the axon initial segment and node of Ranvier, whereas the 190 kDa isoform (AnkG-190) has an emerging role in the dendritic shaft and spine heads. All isoforms of AnkG undergo palmitoylation, a post-translational modification regulating protein attachment to lipid membranes. However, palmitoylation of AnkG-190 has not been investigated in dendritic spines. The ANK3 gene and altered expression of AnkG proteins are associated with a variety of neuropsychiatric and neurodevelopmental disorders including bipolar disorders and are implicated in the lithium response, a commonly used mood stabilizer for bipolar disorder patients, although the precise mechanisms involved are unknown. Here, we showed that Cys70 palmitoylation stabilizes the localization of AnkG-190 in spine heads and at dendritic plasma membrane nanodomains. Mutation of Cys70 impairs AnkG-190 function in dendritic spines and alters PSD-95 scaffolding. Interestingly, we find that lithium reduces AnkG-190 palmitoylation thereby increasing its mobility in dendritic spines. Finally, we demonstrate that the palmitoyl acyl transferase ZDHHC8, but not ZDHHC5, increases AnkG-190 stability in spine heads and is inhibited by lithium. Together, our data reveal that palmitoylation is critical for AnkG-190 localization and function and a potential ZDDHC8/AnkG-190 mechanism linking AnkG-190 mobility to the neuronal effects of lithium.

neuroscience↗

Seascape genetics at its finest: dispersal patchiness within a well-connected population

Dispersal is a main determining factor of population structure and variation. In the marine habitat, well-connected populations with large numbers of reproducing individuals are common but even so population structure can exist on a small-scale. Variation in dispersal between populations or over time is often associated to both environmental and genetic variation. Nonetheless, detecting structure and dispersal variation on a fine-scale within marine populations still remains a challenge. Here we propose and use a novel approach of combining a clustering model, early-life history trait information from fish otoliths, spatial coordinates and genetic markers to detect very fine-scale dispersal patterns. We collected 1573 individuals (946 adults and 627 juveniles) of the black-faced blenny across a small-scale (2km) coastline as well as at a larger-scale area (<50kms). A total of 178 single nucleotide polymorphism markers were used to evaluate relatedness patterns within this well-connected population. Local retention and/or dispersal varied across the 2km coastline with higher frequency of SHORT-range disperser adults; representing local recruitment; towards the southwest of the area. An inverse pattern was found for juveniles, showing an increase of SHORT-range dispersers towards the northeast. This reveals a complex but not full genetic mixing and suggests oceanic/coastal circulation as the main driver of this fine-scale chaotic genetic patchiness within this otherwise homogeneous population. When focusing on the patterns within one recruitment season, we found large differences in temperatures (from approx. 17oC to 25oC) as well as pelagic larval duration (PLD) for juveniles from the beginning of the season and the end of the season. We were able to detect fine-scale differences in HIGH-range juvenile dispersers, representing distant migrants, depending on whether they were born at the beginning of the season, hence, with a longer PLD, or at the end of the reproductive season. The ability to detect such fine-scale dispersal patchiness will aid in our understanding of the underlying mechanisms of population structuring and chaotic patchiness in a wide range of species even with high potential dispersal abilities.

ecology↗

Sex-dependent dominance maintains migration supergene in rainbow trout

Traits with different fitness optima in males and females cause sexual conflict when they have a shared genetic basis. Heteromorphic sex chromosomes can resolve this conflict and protect sexually antagonistic polymorphisms but accumulate deleterious mutations. However, many taxa lack differentiated sex chromosomes, and how sexual conflict is resolved in these species is largely unknown. Here we present a chromosome-anchored genome assembly for rainbow trout (Oncorhynchus mykiss) and characterize a 56 Mb double-inversion supergene that mediates sex-specific migration through sex-dependent dominance, a mechanism that reduces sexual conflict. The double-inversion contains key photosensory, circadian rhythm, adiposity, and sexual differentiation genes and displays frequency clines associated with latitude and temperature, revealing environmental dependence. Our results constitute the first example of sex-dependent dominance across a large autosomal supergene, a novel mechanism for sexual conflict resolution capable of protecting polygenic sexually antagonistic variation while avoiding the homozygous lethality and deleterious mutation load of heteromorphic sex chromosomes.

evolutionary biology↗

Disruption of The Psychiatric Risk Gene Ankyrin 3 Enhances Microtubule Dynamics Through GSK3/CRMP2 Signaling

The ankyrin 3 gene (ANK3) is a well-established risk gene for psychiatric illness, but the mechanisms underlying its pathophysiology remain elusive. We examined the molecular effects of disrupting brain-specific Ank3 isoforms in mouse and neuronal model systems. RNA sequencing of hippocampus from Ank3+/- and Ank3+/+ mice identified altered expression of 282 genes that were enriched for microtubule-related functions. Results were supported by increased expression of microtubule end-binding protein 3 (EB3), an indicator of microtubule dynamics, in Ank3+/- mouse hippocampus. Live-cell imaging of EB3 movement in primary neurons from Ank3+/- mice revealed impaired elongation of microtubules. Using a CRISPR-dCas9-KRAB transcriptional repressor in mouse neuro-2a cells, we determined that repression of brain-specific Ank3 increased EB3 expression, decreased tubulin acetylation, and increased the soluble:polymerized tubulin ratio, indicating enhanced microtubule dynamics. These changes were rescued by inhibition of glycogen synthase kinase 3 (GSK3) with lithium or CHIR99021, a highly selective GSK3 inhibitor. Brain-specific Ank3 repression in neuro-2a cells increased GSK3 activity (reduced inhibitory phosphorylation) and elevated collapsin response mediator protein 2 (CRMP2) phosphorylation, a known GSK3 substrate and microtubule-binding protein. Pharmacological inhibition of CRMP2 activity attenuated the rescue of EB3 expression and tubulin polymerization in Ank3 repressed cells by lithium or CHIR99021, suggesting microtubule instability induced by Ank3 repression is dependent on CRMP2 activity. Taken together, our data indicate that aNK3 functions in neuronal microtubule dynamics through GSK3 and its downstream substrate CRMP2. These findings reveal cellular and molecular mechanisms underlying brain-specific ANK3 disruption that may be related to its role in psychiatric illness.

neuroscience↗

Stronger effects of heterozygosity on survival in harsherenvironments

A stronger correlation between heterozygosity and fitness or its components (e.g., life-history traits such as survival, growth, morphology) is expected in harsher environments, but few studies have investigated whether the effects of heterozygosity on life-history traits vary with environmental conditions in natural populations. Here, the hypothesis that the effects of heterozygosity vary with environmental conditions was tested using six populations of marble trout Salmo marmoratus from Western Slovenia as a model system. Specifically, the tested hypotheses were: stronger effects of heterozygosity on survival in populations characterized by low average survival, no effects of heterozygosity on probability of surviving flash floods owing to their largely non-selective effects across traits, and stronger effects of heterozygosity on survival for fish born after floods than fish born before. A significant effect of heterozygosity on survival was found in populations characterized by low average survival. There were no effects of heterozygosity on probability of surviving flash floods, but in one population a positive correlation between heterozygosity and survival for fish born after the extreme events was found, probably because crowding in a small section of the stream caused more intense competition for resources.

ecology↗

Effects of species invasion on population dynamics, vital rates, and life histories of the native species

Invasions occurring in natural environments provide the opportunity to study how vital rates change and life histories evolve in the presence of a competing species. In this work, we estimate differences in reproductive traits, individual growth trajectories, survival, life histories, and population dynamics between a native species living in allopatry and in sympatry with an invasive species of the same taxonomic Family. We used as a model system marble trout Salmo marmoratus (native species) and rainbow trout Oncorhynchus mykiss (non-native) living in the Idrijca River (Slovenia). An impassable waterfall separates the stream in two sectors only a few hundred meters apart: a downstream sector in which marble trout live in sympatry with rainbow trout and a upstream sector in which marble trout live in allopatry. We used an overarching modeling approach that uses tag-recapture and genetic data (> 2,500 unique marble and rainbow trout were sampled and SNP-genotyped) to reconstruct pedigrees, test for synchrony of population dynamics, and model survival and growth while accounting for individual heterogeneity in performance. The population dynamics of the two marble trout populations and of rainbow trout were overall synchronous. We found higher prevalence of younger parents, higher mortality, and lower population density in marble trout living in sympatry with rainbow trout than in marble trout living in allopatry. There were no differences in the average individual growth trajectories between the two marble trout populations. Faster life histories of marble trout living in sympatry with rainbow trout are consistent with predictions of life-history theory.

ecology↗