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Bell, M. A.

Publications and source records attributed to Bell, M. A..

7 recordsLinked to original sources

Variable jackpot individuals provide most alleles for repeated, rapid adaptation to freshwater by anadromous Threespine Stickleback

Experimental introductions of anadromous stickleback into freshwater habitats lacking this species allow analysis of the process of adaptation to freshwater forward-in-time. We examined the population genomic dynamics during early stages of adaptation in three replicate lakes that were experimentally founded, each using [~]3000 anadromous ancestors. We replicated earlier results that rare individuals carrying large haploblocks of freshwater-adaptive alleles (jackpot carriers) provide most of the allelic variation for adaptation of anadromous Threespine Stickleback to freshwater within only a few generations in each lake. There were population bottlenecks two to three generations after founding in each lake, after which jackpot carriers dramatically increased in frequency and came to dominate the populations. Individuals lacking large adaptive haploblocks experienced low fitness in their new freshwater environments, consistent with our previous report based on a single lake population. Despite similarities of the demographic responses to selection, the alleles that were most common among jackpot carriers were different in each population, suggesting that each lake population likely adapted to conditions in freshwater environments through different genes. These results provide direct evidence for the genomic mechanisms underlying the rapid adaptation of anadromous sticklebacks to freshwater environments, a process that can occur within just a few generations.

evolutionary biology↗

Rapid and repeated evolution of myosin copy number in threespine stickleback

Copy number variants at genomic loci evolve at a high rate, are linked to many different diseases, and play a role in adaptive evolution in humans and other organisms. Here we show that stickleback fish from freshwater environments have rapidly and repeatedly evolved an expanded number of copies of a gene family involved in muscle development, Myosin Heavy Chain 3 Cluster C (MYH3C), compared to marine populations. Differences in copy number between marine and freshwater fish are maintained even in the presence of gene flow, suggesting that MYH3C changes represent adaptive divergence between ecotypes. Copy number expansion occurs by tandem duplication of MYH3C coding and regulatory regions on the stickleback sex chromosome. We identify a muscle regulatory enhancer within the expanded MYH3C region and show that elevated copy number is associated with developmental and tissue-specific increases in corresponding mRNA expression levels in skeletal muscle. Common MYH3C clusters include 3-, 4-, 5-, and 6-copy variants that likely evolved through a combination of microhomology-mediated break repair and non-allelic homologous recombination. Our results provide a new example of copy number changes in a wild species and identify CNVs as potential "hotspots" of repeated adaptive evolution.

evolutionary biology↗

Rare Jackpot Individuals Drive Rapid Adaptation in Threespine Stickleback

Recombination has long been considered the primary mechanism to bring beneficial alleles together, which can increase the speed of adaptation from standing genetic variation. Recombination is fundamental to the transporter hypothesis proposed to explain precise parallel adaptation in Threespine Stickleback. We studied an instance of freshwater adaptation in the Threespine Stickleback system using whole genomic data from an evolutionary time series to observe the genomic dynamics underlying rapid parallel adaptation. Our experiment showed that rapid adaptation to a freshwater environment depended on a few individuals with large haploblocks of freshwater-adaptive alleles (jackpot carriers) present among the anadromous (i.e., sea-run) founders at low frequencies. Biological kinship analyses indicate that mating among jackpot carriers and between jackpot carriers and non-jackpot individuals led to a rapid increase in freshwater-adaptive alleles within the first few generations. This process allowed the population to overcome a substantial bottleneck likely caused by the low fitness of first-generation stickleback with a few freshwater-adaptive alleles born in the lake. Additionally, we found evidence that the genetic load that emerged from population growth after the bottleneck may have been reduced through an increase in homozygosity by inbreeding, ultimately purging deleterious alleles. Recombination likely played a limited role in this case of very rapid adaptation.

evolutionary biology↗

Genome Sequence of a Marine Threespine Stickleback (Gasterosteus aculeatus) from Rabbit Slough in the Cook Inlet

The Threespine Stickleback, Gasterosteus aculeatus, is an emerging model system for understanding the genomic basis of vertebrate adaptation. A strength of the system is that marine populations have repeatedly colonized freshwater environments, serving as natural biological replicates. These replicates have enabled researchers to efficiently identify phenotypes and genotypes under selection during this transition. While this repeated adaptation to freshwater has occurred throughout the northern hemisphere, the Cook Inlet in south-central Alaska has been an area of focus. The freshwater lakes in this area are being studied extensively and there is a high-quality freshwater reference assembly from a population in the region, Bear Paw Lake. Using a freshwater reference assembly is a potential limitation because genomic segments are repeatedly lost during freshwater adaptation. This scenario results in some of the key regions associated with marine-freshwater divergence being absent from freshwater genomes, and therefore absent from the reference assemblies. It may also be that isolated freshwater populations are more genetically diverged, potentially increasing reference biases. Here we present a highly-continuous marine assembly from Rabbit Slough in the Cook Inlet. All contigs are from long-read sequencing and have been ordered and oriented with Hi-C. The contigs are anchored to chromosomes and form a 454 Mbp assembly with an N50 of 1.3 Mbp, an L50 of 95, and a BUSCO score over 97%. The organization of the chromosomes in this marine individual is similar to existing freshwater assemblies, but with important structural differences, including the 3 previously known inversions that repeatedly separate marine and freshwater ecotypes. We anticipate that this high-quality marine assembly will more accurately reflect the ancestral population that founded the freshwater lakes in the area and will more closely match most other populations from around the world. This marine assembly, which includes the repeatedly deleted segments and offers a closer reference sequence for most populations, will enable more comprehensive and accurate computational and functional genomic investigations of Threespine Stickleback evolution.

genomics↗

Evolution of stickleback spines through independent cis-regulatory changes at HOXDB

Understanding the genetic mechanisms leading to new traits is a fundamental goal of evolutionary biology. We show that HOXDB regulatory changes have been used repeatedly in different stickleback fish species to alter the length and number of bony dorsal spines. In Gasterosteus aculeatus, a variant HOXDB allele is genetically linked to shortening an existing spine and adding a spine. In Apeltes quadracus, a variant allele is associated with lengthening an existing spine and adding a spine. The alleles alter the same conserved non-coding HOXDB enhancer by diverse molecular mechanisms, including SNPs, deletions, and transposable element insertions. The independent cis-acting regulatory changes are linked to anterior expansion or contraction of HOXDB expression. Our findings support the long-standing hypothesis that natural Hox gene variation underlies key morphological patterning changes in wild populations and illustrate how different mutational mechanisms affecting the same region may produce opposite gene expression changes with similar phenotypic outcomes. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=154 SRC="FIGDIR/small/472698v1_ufig1.gif" ALT="Figure 1"> View larger version (32K): org.highwire.dtl.DTLVardef@8e6675org.highwire.dtl.DTLVardef@e89e13org.highwire.dtl.DTLVardef@1e1f1dcorg.highwire.dtl.DTLVardef@cdb6f8_HPS_FORMAT_FIGEXP M_FIG C_FIG

evolutionary biology↗

Predicting future from past: The genomic basis of recurrent and rapid stickleback evolution

Similar forms often evolve repeatedly in nature, raising longstanding questions about the underlying mechanisms. Here we use repeated evolution in sticklebacks to identify a large set of genomic loci that change recurrently during colonization of new freshwater habitats by marine fish. The same loci used repeatedly in extant populations also show rapid allele frequency changes when new freshwater populations are experimentally established from marine ancestors. Dramatic genotypic and phenotypic changes arise within 5-7 years, facilitated by standing genetic variation and linkage between adaptive regions. Both the speed and location of changes can be predicted using empirical observations of recurrence in natural populations or fundamental genomic features like allelic age, recombination rates, density of divergent loci, and overlap with mapped traits. A composite model trained on these stickleback features can also predict the location of key evolutionary loci in Darwins finches, suggesting similar features are important for evolution across diverse taxa.

evolutionary biology↗

Intercontinental genomic parallelism in multiple adaptive radiations

Parallelism, the evolution of similar traits in populations diversifying in similar conditions, provides good evidence of adaptation by natural selection. Many studies of parallelism have focused on comparisons of strongly different ecotypes or sharply contrasting environments, defined a priori, which could upwardly bias the apparent prevalence of parallelism. Here, we estimated genomic parallelism associated with individual components of environmental and phenotypic variation at an intercontinental scale across four adaptive radiations of the three-spined stickleback (Gasterosteus aculeatus), by associating genome-wide allele frequencies with continuous distributions of environmental and phenotypic variation. We found that genomic parallelism was well predicted by parallelism of phenotype-environment associations, suggesting that a quantitative characterization of phenotypes and environments can provide a good prediction of expected genomic parallelism. Further, we examined the explanatory power of genetic, phenotypic, and environmental similarity in predicting parallelism. We found that parallelism tended to be greater for geographically proximate, genetically similar radiations, highlighting the significant contingency of standing variation in the early stages of adaptive radiations, before new mutations accumulate. However, we also demonstrate that distance within multivariate environmental space predicts parallelism, after correction for genetic distance. This study thus demonstrates the relative influences of environment, phenotype and genetic contingency on repeatable signatures of adaptation in the genome.

evolutionary biology↗