Interview with the author: Dynamics of genomic change during evolutionary rescue in the seed beetle Callosobruchus maculatus

We interviewed graduate student Alexandre Rêgo and Professor Zach Gompert from Utah State University about their work on evolutionary rescue in seed beetles where they explore how demographic history affects parallel evolution at the genetic level. Their results have important implications for or understanding of repeatability and predictability of evolution. Read the full text below:

Alexandre Rêgo, Frank J. Messina, and Zachariah Gompert. (2019) Dynamics of genomic change during evolutionary rescue in the seed beetle Callosobruchus maculatus. https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.15085?af=R

Drawing of C. maculatus (by Amy Springer)
Drawing of Callosobruchus maculatus (by Amy Springer)


What led to your interest in this topic / what was the motivation for this study?

(AR and ZG) We were interested in evolutionary rescue, that is in cases where population decline and extinction in a marginal or stressful environment is halted and reversed by adaptive evolution. We were especially interested in what patterns of change and natural selection look like across the genome during rescue. How many genes are involved? How much do gene/allele frequencies change? And how fast? We turned to an evolve-and-resequence experiment with Callosobruchus maculatus seed beetles for this. Past work has shown that these beetles can barely survive on lentils (survival rates are ~1%), but that they sometimes can rapidly adapt and persist on this novel host (survival rates can climb to 80 or 90% in fewer than 20 generations).

What difficulties did you run into along the way?

(AR and ZG) Extinction. We were drawn to this system because of the potential for adaptation or extinction, and because of the related extraordinary pace and degree of adaptation when it occurs. We wanted to measure selection and genome-wide evolutionary change during evolutionary rescue, but (for better and worse) only one of 10 replicate lines was rescued. This limited our ability to assess parallelism during rescue, but also highlighted how real the possibility of extinction (in the absence of rapid adaptation) is in this system.

What is the biggest or most surprising finding from this study?

(AR and ZG) We were most shocked by just how rapid evolutionary changes were at the molecular level. We saw numerous cases where allele frequencies at multiple (albeit not always independent) genetic loci shifted by 20-40% or more in a single generation. This is really much more extreme than rates of change often considered.

Moving forward, what are the next steps for this research?

(AR and ZG) We are taking our work on C. maculatus in two directions. First, we have finished creating and sequencing crosses between the lentil adapted and source populations to identify genetic variants associated with specific fitness components (e.g., development time and adult size) on lentil. This will make a nice comparison with the selection scans. Second, we are now working with additional populations, some of which do a bit better on lentil, to examine consistency in genomic change across lines in lentil adaptation and to figure out whether hybridization facilitates adaptation to this marginal host.

Adult C. maculatus on their ancestral host, mung bean.

What would your message be for students about to start their first research projects in this topic?

(AR) Attention to detail is critical. Be as careful as possible in how you plan and organize your data on analyses. Population genomic analyses, especially with approximate Bayesian computation, generate an inordinate amount of output. And you will almost certainly want to re-run things with slightly different parameters, etc., so carefully documenting everything is critical.

What have you learned about science over the course of this project?

(AR) There are many things that must be done in order to complete a study, each requiring a different set of skills. As a graduate student, it can be daunting to acquire and become proficient at so many things. However, at the end of this study, I can look back and see that I have made progress as a scientists on many fronts. What I’ve learned from this project has provided me a solid foundation for my current studies on which I can further improve.

Describe the significance of this research for the general scientific community in one sentence.

(AR and ZG) Very rapid adaptation is possible when species or populations find themselves in harsh environments, sometimes this is enough to prevent extinction, and sometimes it isn’t.

Describe the significance of this research for your scientific community in one sentence.

(AR and ZG) Population genomic patterns associated with evolutionary rescue differ in subtle and not so subtle ways from patterns observed in other situations involving less extreme or softer selection, and thus warrant more study and consideration.

Interview with the author: Integrating life history traits into predictive phylogeography

In this exciting research, Jack Sullivan and Megan Smith and colleagues use machine learning techniques to create a powerful predictive framework for phylogeographic studies. Learn about their experiences building this novel research approach!

What led to your interest in this topic / what was the motivation for this study? 
We’ve been interested in the question of whether or not we can predict phylogeographic patterns for some time. Initially, we attempted to predict whether or not unstudied species harbored cryptic diversity using climate and taxonomic information (https://royalsocietypublishing.org/doi/pdf/10.1098/rspb.2016.1529). We used taxa that were known to either harbor or lack cryptic diversity to train a Random Forest classifier, and then made predictions about unstudied taxa. We found that we could predict the presence or absence of cryptic diversity (with low error rates when based on cross-validation!) We also saw that taxonomy was a powerful predictor of cryptic diversity, and we began to wonder why. In this study, we evaluate whether life history traits can explain this result.

What difficulties did you run into along the way? 
When trying to use life history traits to make predictions across taxonomic levels, the most difficult problem is finding appropriate traits. Many traits, while likely very informative for specific taxa, are difficult to score across taxonomic groups. Our dataset included mammals, plants, arthropods, gastropods, amphibians, and birds. The biggest difficulty was finding life history traits that we could score across all of these groups and that we hypothesized would be meaningful predictors of phylogeographic patterns.

What is the biggest or most surprising finding from this study? 
Life history traits are great predictors of phylogeographic patterns. In one of the systems we studied, these traits can even replace taxonomy as a predictor, suggesting that taxonomy was serving as a proxy for these traits. We find that traits related to reproduction (e.g. reproductive mode, clutch size) and trophic level are particularly informative in our predictive framework.

The reticulate taildropper slug (Prophysaon andersoni), like many other invertebrates from the rainforests of the Pacific Northwest, lacks deep divergence between inland and coastal rainforest populations.

Moving forward, what are the next steps for this research? 
There is a wealth of data on phylogeographic patterns available, but most studies have focused on one or a few species. The framework developed in Espíndola et al. (2016) and expanded upon here provides a mechanism for integrating these studies into a predictive framework. As data continue to become available, our approach will allow policymakers and scientists alike to make predictions about what patterns are expected in unstudied species. Further, this approach can provide insight into which life history traits drive differences in species responses to historic events, and this may allow us to begin to understand why species respond to similar events in idiosyncratic ways.

What would your message be for students about to start their first research projects in this topic? 
Think early and often about how your work can be integrated into the field in a broader way. Particularly as molecular data become easier to collect, more and more single species studies accumulate. By looking at these studies in a new light and integrating across studies, we can learn a lot about communities and overarching patterns.

What have you learned about science over the course of this project? 
Over the course of this project, I’ve learned to look at data in many different ways. Our initial work on this topic suggested that taxonomy was the most important predictor of phylogeographic patterns. While true, this told us little about the biology of the taxa we were studying. By delving deeper and adding life history traits to our study we were able to draw biologically meaningful conclusions about why species responded differently to geologic and climatic events.

We used our predictive framework to understand cryptic diversity in the temperate rainforests of the Pacific Northwest. Pictured is the Siuslaw National Forest, where many of the temperate rainforest endemics in our study can be found.

Describe the significance of this research for the general scientific community in one sentence.
By using machine learning, we can integrate genomic, ecological, and trait data to make predictions about how species have responded to historic events, and to understand which factors lead to idiosyncratic responses.

Describe the significance of this research for your scientific community in one sentence.
Using publicly available data and machine learning techniques, we can make predictions about phylogeographic patterns across broad taxonomic groups, and we can draw conclusions about how life history traits influence these patterns.

Summary from the authors: A reciprocal translocation radically reshapes sex‐linked inheritance in the common frog

Sex chromosomes evolve when recombination ceases between the X and Y chromosomes, and the X and Y chromosome accumulate differences between them. We examined sex chromosomes across three populations of the common frog, Rana temporaria. In one population, we confirm that the sex chromosome and an autosome have undergone a reciprocal translocation, a rearrangement in which two chromosomes swap arms. The resulting chromosome pair is coinherited as sex chromosomes. Furthermore, because frog chromosomes only recombine near the ends, much of the newly added chromosome is incorporated into the sex-determining region. This provides a large amount of new genetic material to the selective environment of the sex chromosomes, in which sequence on the X chromosome are under selection in females twice as often as males, and sequence on the Y are subject sex-specific selection in males. We further confirmed unique sex-chromosome arrangements in the other two populations, demonstrating that Rana temporaria has extensive structural polymorphism in its sex chromosomes. — Melissa Toups

Toups, M., Rodrigues, N, Perrrin, N, and M. Kirkpatrick. (2019). Genomics, environment and balancing selection in behaA reciprocal translocation radically reshapes sex‐linked inheritance in the common frog. Molecular Ecology28(8), 1877–1889. https://doi.org/10.1111/mec.14990

Interview with the author: A reciprocal translocation radically reshapes sex‐linked inheritance in the common frog

In this Blog post, we hear from Dr. Melissa Toups on how new sex chromosomes can evolve! Mellisa and her colleagues show that reciprocal translocations can incorporate large pieces of chromosome into a sex-determining region, thus making the to be co-inherited as sex chromosomes. Join us in learning more about this exciting research directly from Mellisa.

Picture by Christophe Dufresnes

What led to your interest in this topic / what was the motivation for this study? 
I’m interested in the diversity of genetic sex-determination mechanisms. Ranid frogs are a fantastic study species for this because sex determination moves between chromosomes on a fast evolutionary time scale. In Rana temporaria, the study species for this paper, sex chromosome arrangements differ between populations.  We knew from previous linkage maps using microsatellites that the southernmost population had only one small sex-determining region, one northern population had one a larger sex-determining region on the same chromosome, and finally a second northern population had two sex chromosomes formed by reciprocal translocation, which occurs when two chromosomes swap arms and become coinherited.  This was a great opportunity to use genomic techniques to study three different arrangements of sex chromosomes within a single species.

What difficulties did you run into along the way? 
During breeding season, frogs migrate to nearby ponds.  In the evening, the males swim around and sing to females. The successful males attach to females, and we catch them as a couple.  The two northernmost populations, Kilpisjärvi and Ammarnas, breed at the roughly the same time.  We started in Ammarnas, but catching the frogs we needed took longer than expected.  By the time we arrived in Kilpisjärvi, breeding season was almost over.  Most of the frogs remaining in the ponds were single males. We were only able to catch two breeding pairs, and we were lucky enough to eventually find two solo females, but it took weeks of effort, which was nerve-wracking. \

What is the biggest or most surprising finding from this study? 
We are the first to use genomic techniques to characterize a reciprocal translocation of a sex chromosome. We don’t know how common these rearrangements are because they are only cytologically detectable at pairing during meiosis.  Here, we show that they can incorporate large regions of an additional chromosome into the sex-determining region, which are subject to very different selective forces than the autosomes.  The most surprising finding was detecting evidence for another small nonrecombining region in Kilpisjärvi on a different chromosome. These frogs are full of surprises!

Moving forward, what are the next steps for this research?
We are currently investigating whether different sex chromosome arrangements affect male gene expression.  To answer this question, we are focusing on an alpine population of Rana temporaria in Switzerland that has males with two types of Y chromosomes.  Some Y chromosomes only differ from the X chromosome in a small region around the sex-determining locus, and other Y chromosomes are differentiated from the X chromosome throughout their length. We are also working on using high-density linkage mapping of RAD sequences to confirm the novel sex-chromosome rearrangement in the Kilpisjärvi populations.

What would your message be for students about to start their first research projects in this topic? 
Our standard models for sex-chromosome evolution are mostly based on the mammalian XY system, which are more than 160 million years old.  However, the more organisms we study, the more we realize that ancient, highly diverged sex chromosomes may be the exception rather than the rule. My message would be to keep an open mind about what you might find, and let your organism surprise you!

What have you learned about science over the course of this project? 
One thing I’ve learned working on this project is the importance of assembling a team of researchers with complementary strengths.  Each person brought unique and critical skills to this project. We were able to combine knowledge of our study system, bioinformatics, and coalescent modeling to produce a comprehensive examination at sex chromosomes in Rana temporaria.

Describe the significance of this research for the general scientific community in one sentence.
We provide the first genomic view of an entirely different way that new sex chromosomes can evolve.

Describe the significance of this research for your scientific community in one sentence.
We show that the reciprocal translocations can dramatically increase the portion of the genome that is incorporated into the sex-determining region.