Chromosomal Inversions and Omy05

Image description: chromosomal inversion depicted by orange and blue blobs with different species morphs that result from chromosomal inversions. Steelhead and rainbow trout (Oncorhynchus mykiss) are featured, as well as two white-throated sparrows (Zonotrichia albicollis), three walking stick insects (Timema cristinae), three numata longwing butterflies (Heliconius numata), and silver-leafed (Helianthus argophyllus) and cultivated (Helianthus annuus) sunflower species.

My current work focuses on Oncorhynchus mykiss, steelhead and rainbow trout, and how genetic and epigenetic influences affect life history. Put more simply, I’m studying how a juvenile O.mykiss’ genetics influence if that individual will become a steelhead or rainbow trout. Steelhead and rainbow trout are both ecotypes of the same species of salmonid, but they look and behave very differently. Both steelhead and rainbow trout hatch and eventually will spawn and die in freshwater streams, but only steelhead undergo a complex process called “smoltification” that allows them to successfully transition from freshwater to saltwater- allowing them to migrate to sea and return to freshwater to spawn. When migrating back to freshwater rivers from the ocean, steelhead also bring essential nutrients and elements from marine to freshwater habitats. Steelhead are struggling in their native ranges from barriers to anadromy, such as dams. Hatcheries, like the one I work with for this project, aim to mitigate steelhead losses from lost spawning habitat by supplementing produced fish. Understanding the molecular mechanisms behind anadromy is not only an interesting evolutionary question, but it could be potentially useful for conservation.

To discuss this project more in-depth once results shake out, I’ve created a quick primer on chromosomal inversions and their relevance to O.mykiss. My dissertation project focuses specifically on a previously, yet repeatedly identified, “supergene” referred to as Omy05. This inversion has been significantly associated with life history expression (if a fish will be a migrant steelhead or resident rainbow trout). Before I go into what we know about this inversion so far and what my project is looking into specifically, let’s explore chromosomal inversions more and why inversions are so important to studying molecular adaptation, or how genetics are involved in species adapting to their environment.

Figure 1: Depiction of close up of inverting chromosome. A chunk of chromosome breaks off, flips orientation, and reinserts itself back into the chromosome. Recombination during meiosis is not able to break up the inversion, so it moves as a unit through generations. The genes caught within the inversion are subjected to selection as a single group, in contrast with the genes left outside the inversion. This allows for the evolution and molding of complex traits.

What are chromosomal inversions again?

If you looked at my post about genetics basics, you probably remember that mutations happen at different levels in the genetic material of all living things on Earth. Chromosomal inversions occur when a piece of chromosome breaks off, flips, then reinserts itself (Figure 1). This is important because this effectively locks all the genes contained in that region in place, so they cannot be shuffled apart during recombination. Genes blocked off together are then selected against as a single unit and coevolve together. As molecular technology advances and sequencing costs decline, more chromosomal inversions are being identified that play important roles in molecular adaptation.

ok.. Why do they matter?

Variation is a crucial component to evolution of traits - including variations in molecular structure. Chromosomal inversions have already been found in a variety of complex life history (ie timing of reproduction and death) systems. Different inversion variations in a population can maintain complex, distinct phenotypes by containing large blocks of genes that cannot recombine during meiosis. Suppressing recombination prevents selection from acting on new variations of those gene blocks, but allows selection to act on those genes as a single unit. Locking genes together can lead to the development of complicated, environmentally-adapted traits. They have even been suggested to be behind some speciation events by causing reproductive barriers between different species members. These speciation events have mainly found in plants, as plants are a lot more “go with the flow” when it comes to sudden genetic changes.

This review by Wellenreuther and Bernatchez (2018) in Trends in Ecology & Evolution (citation below) summarizes everything way better than I have here, but there are a couple examples they highlighted that I found really interesting! I drew these species out in the image for this post to show some of the gorgeous variation in species characteristics and behaviors.

Cool Inversion Examples:

• speciation:

  • example: sunflowers Helianthus argophyllus (silver-leafed) and Helianthus annuus (cultivated) - inversion associated with different life history characteristics leading to formation of different species

• mating - ie alternate mating strategies

  • example: white-throated sparrow Zonotrichia albicollis- inversion associated with different reproductive and parenting strategies

• environmental adaptation

  • example: stick insects Timema cristinae- inversion associated with colors for camouflage

  • example: butterflies Heliconius numata- inversion associated with wing patterns

• behavior

  • example: Omy05 in steelhead/rainbow trout! -inversion associated with life history expression (migrant or resident)

Omy05

Omy05 acts as a supergene: it contains multiple genes that work together to create a complex trait: migration or residency. The effects of Omy05 on life history depend on genotype (AA, AR, RR), but also on temperature, migration barriers and individual sex.

There are a lot of different factors that influence life history expression in O.mykiss, but the big ones are genetics, the environment, and the individual’s condition (sex, how big/fat). Because migration is such a plastic trait in O.mykiss, it is a bit challenging to make sense of all the different data scientists have collected, but some clear patterns have emerged. Omy05 is a chromosomal inversion strongly affiliated with anadromy in O.mykiss. It contains over a thousand genes, some of which have been strongly associated with development speed (affects how big is possible). It isn’t the only important molecular structure for life history in O.mykiss by any means, but it has been repeatedly associated with significant life history traits. Fish with Omy05 AA genotypes are typically more likely to be steelhead and RR genotypes are more likely to be rainbow trout. That makes sense, maybe even seems tidy?

Surprise! We have another genotype: AR - which has fish migrating or residing in freshwater. It’s harder, but when you consider sex, female fish with AR genotypes are more likely to become steelheads, while AR males are more likely to be rainbow trout. These differences stem from differences in reproductive strategies between male and female fish. Females have higher fecundity with greater size- it’s more beneficial for females to migrate and become as big as possible before spawning. She increases her number of offspring by increasing her of eggs, which means she has to increase her body’s capacity for holding eggs. Males can have high success at smaller sizes, as milt is much cheaper to manufacture than eggs. By investing energy in maximal growth towards sexual maturity, he can maximize his success by starting spawning earlier.

If this isn’t complicated enough (and I’m not even going to touch on iteroparity vs. semelparity in these guys aka spawning many times or only spawning once and dying), the environment also throws some curveballs. The biggest impact on if an O.mykiss population features migration is if that population has access to saltwater or not - landlocked fish are not going to magically migrate unfortunately. Beyond that, there are other interesting environmental effects, specifically water temperature. Rainbow trout are typically found in cooler water than steelhead. For Omy05 specifically, there is a latitudinal cline across their natural range from southern California to Alaska that features more RR type fish up North and more AAs down South.

I’m running some experimental rearing at Mokelumne River Hatchery by creating intentional offspring from parents with known Omy05 genotypes from hatchery broodstock. I’d love to run some temperature-controlled experiments to dig into the influence of temperature on Omy05 function. We’re getting ready to enter our third year this winter, so we are already seeing interesting phenotypic differences in our experimental fish. Hopefully more updates to come!

References:

Wellenreuther, Maren & Bernatchez, Louis. (2018). Eco-Evolutionary Genomics of Chromosomal Inversions. Trends in Ecology & Evolution. 33. 10.1016/j.tree.2018.04.002.