Using surfperches to help understand the genomic basis of divergence and local adaptation

Gary Longo is a graduate student in Ecology and Evolutionary Biology, in the Bernardi lab, at UC Santa Cruz. Gary introduces his work on the Embiotocidae in the guest post below.

I became interested in the molecular evolution of fishes while taking an undergraduate Ichthyology course. I was majoring in both marine biology and molecular cell & developmental biology and wasn’t sure which direction I wanted to take my education. On one hand I was interested in molecular biology and particularly fascinated by DNA.

Not only does DNA serve as the blueprint for all living organisms, it also records many aspects of each lineage’s history.

There is so much information encrypted in those four nucleotide bases (i.e. ACGT) just waiting to be extrapolated with the right tools. On the other hand, I was drawn to marine life and had a particular soft spot for fishes. Not only are they the most beautiful and charismatic organisms in the water (personal observation), they are by far the most diverse group of vertebrates (33,265 described spp. and counting). In fact all terrestrial vertebrate diversity (i.e., birds, reptiles, amphibians, and mammals) descend from ancestral lineages of lobe-finned fishes, which are related to the extant lungfish and coelacanth. Over the last 500 million years, fishes have diversified and evolved a mixed bag of adaptations, morphologies, and life history strategies. Indeed, this amazing diversity has enticed many researchers to utilize fish as model systems to tackle an equally diverse array of questions. So when my ichthyology professor (and future advisor) Dr. Giacomo Bernardi began describing the application of molecular techniques to studying the ecology and evolution of fishes, I was drawn to the prospect of combining the fields.

I first had to decide how I was going to utilize DNA to study fishes in graduate school. There are two factors that warrant some thought when starting a research project. The first is what questions do you want ask? The second is what system you want to use to address these questions? In many cases, researchers are strongly interested in one factor and choose the other based on what really floats their boat. For me, I chose surfperches (Embiotocidae) as a model system to investigate how selection operates at the genomic scale. Why? Well if Steve hasn’t convinced you yet, surfperches are an amazing group of fish with unique life history traits, many of which are conducive to addressing important biological questions such as understanding the genomic response to natural selection. This query is a central interest in evolutionary biology as it sheds light on the molecular mechanisms responsible for adaptation and ultimately speciation.

Recent studies have detected genomic signals of adaptation among populations facing different selective pressures (Hohenlohe et al., 2010; Miller et al., 2012).

Researchers are able to investigate selection by identifying “footprints” left behind in the genome of diverging populations or species.

One way to identify genomic signals of local adaptation is to compare allele frequencies among populations, generate an average FST value (metric of population differentiation based on genetic differences), and identify outliers as candidate loci (Hohenlohe et al., 2010; Lewontin & Krakauer, 1973). I have been focusing on identifying regions of the genome potentially under selection in four species of surfperches in northern versus southern California populations. Importantly, significant differences in abiotic conditions (e.g., sea surface temperatures) between northern and southern California may exert differential selective pressure resulting in local adaptation (Dalziel, Rogers, & Schulte, 2009; Larsen, Schulte, & Nielsen, 2011; Scott, Williams, & Crawford, 2009)

Surfperches in their element

One the most interesting characteristics of surfperches, and the reason why I chose them as my study system, is their reproductive strategy of mating via internal fertilization and giving birth to live young. This differs from most marine fishes, which exhibit external fertilization and are characterized by pelagic larvae that remain in the open ocean for days to months before recruiting to suitable habitat. Because surfperches lack this pelagic larval phase, movement among populations is restricted to adults and juveniles, limiting the exchange of genes (i.e., gene flow) between distant populations and increasing the likelihood for local adaptation. Initial results indicate there are indeed “footprints” of selection between populations of surfperches in the North versus the South. I am currently working on identifying where in the genome these events are occurring in hopes of identifying which genes are actually under selection. As sea surface temperatures continue to rise, understanding which genes are under selection in surfperches of the warmer waters of southern California may inform us where we can expect selection to act across genomes of other taxa affected by climate change.

In order to accurately understand selection and speciation events within surfperches, I also have been working to resolve interspecies evolutionary relationships among surfperches using phylogenetic inference (comparing similarities and differences in shared genes among species) at a family wide scale. This work uses the same principles that Steve and colleagues used to build a phylogeny for Amphistichin surfperches.

References

Dalziel, A. C., Rogers, S. M., & Schulte, P. M. (2009). Linking genotypes to phenotypes and fitness: how mechanistic biology can inform molecular ecology. Molecular Ecology, 18(24), 4997–5017.

Hohenlohe, P. A., Bassham, S., Etter, P. D., Stiffler, N., Johnson, E. A., & Cresko, W. A. (2010). Population Genomics of Parallel Adaptation in Threespine Stickleback using Sequenced RAD Tags. Plos Genetics, 6(2).

Larsen, P. F., Schulte, P. M., & Nielsen, E. E. (2011). Gene expression analysis for the identification of selection and local adaptation in fishes. Journal of Fish Biology, 78(1), 1–22.

Lewontin, R. C., & Krakauer, J. (1973). DISTRIBUTION OF GENE FREQUENCY AS A TEST OF THEORY OF SELECTIVE NEUTRALITY OF POLYMORPHISMS. Genetics, 74(1), 175–195.

Miller, M. R., Brunelli, J. P., Wheeler, P. a, Liu, S., Rexroad, C. E., Palti, Y., … Thorgaard, G. H. (2012). A conserved haplotype controls parallel adaptation in geographically distant salmonid populations. Molecular Ecology, 21(2), 237–49.

Scott, C. P., Williams, D. a, & Crawford, D. L. (2009). The effect of genetic and environmental variation on metabolic gene expression. Molecular Ecology, 18(13), 2832–43.

If you didn’t get enough of Gary’s underwater surfperch video, you can find more here.

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