Interview with the author: Landscape genomic signatures indicate reduced gene flow and forest‐associated adaptive divergence in an endangered neotropical turtle

The Dahl’s Toad-headed turtle (Mesoclemmys dahli) is one of the 25 most endangered turtle species on Earth and one of the unlucky few that is constantly being compared to a toad. A previous study has shown that extensive habitat conversion and fragmentation in its native range in Colombia has led to genetic differentiation among populations. However, critical questions remain for the conservation and management of this species: how does habitat type and quality in this rapidly changing region influence gene flow? How can genomic data inform the management of this endangered species?

Dr. Natalia Gallego García (@NataGalle) and colleagues set out to answer these questions. Read below for an interview with Natalia about the challenges of working with such a rare species and how this study provides the foundation for a genetic rescue program for the Dahl’s Toad-headed turtle.

The critically endangered Dahl’s Toad‐headed turtle (Mesoclemmys dahli). Photo by N. Gallego García

What led to your interest in this topic / what was the motivation for this study? 
We conducted a previous population genetics study using microsatellite loci on this highly endangered species, in which we found significant genetic evidence of population fragmentation. In this follow-up study, we wanted to know how the current landscape, now composed of open grasslands for cattle instead of tropical dry forest, might be restricting gene flow and thus causing the observed fragmentation. We also wanted to know how this new anthropogenic environment was potentially driving local adaptation.

What difficulties did you run into along the way? 
The main difficulty was finding this rare species across its range to get the samples. Another difficulty was standardizing the RADseq protocol, as our research was the first genomic-level study on any side-necked (pleurodiran) turtle. Also, there is no reference genome for this species or for any closely related one, making the analysis of our data difficult. We had to assembly a de novo genome, which prevented us from running other analyses that could have allowed us to learn more about adaptive mechanisms to new environments.

What is the biggest or most surprising finding from this study? 
First of all, we were able to show that population fragmentation was related to habitat loss. However, we were expecting movement through grasslands to be costly, given that this is a forest species, but we found that from a scale of 1 (easy) to 1000 (hard) the cost of traversing grassland was only 13. We believe that this low cost is associated with the presence of water ponds built in the pastures for the cattle to drink, which are increasingly being used by this species. These ponds might be serving as a sort of stepping stone array of lower quality but still usable aquatic habitat, enabling movement over an otherwise hostile matrix. Our second surprising finding was observing possible adaptive divergence between populations occupying areas with more forest than populations in areas with almost no forest. This result suggests that the populations might be adapting to this new transformed environment. However, adaptation alone is not rescuing this species from the negative effects of fragmentation, and currently the species is facing a high risk of extinction.

Moving forward, what are the next steps for this research?
The next steps can be divided in terms of management and research. In terms of management, we are currently designing a genetic rescue program to reduce inbreeding and increase population genetic diversity, without disrupting the potential ongoing adaptation that we observed. In terms of research, we are currently assembling the genome of a closely related species, which will allow us to map the putatively adaptive loci found, and better understand how this species is adapting to its new transformed environment. This will also allow us to design a field and/or laboratory experiment to further explore the possibility of adaptation to altered, and degraded habitat.

What would your message be for students about to start their first research projects in this topic? 
Working with non-model, rare, and threatened organisms, although challenging, can lead to valuable information that is vital in their conservation. So, accept the challenge and stand up for those forgotten species. Any new information on a data deficient species will increase its chance of survival, which in itself already makes the research worthwhile.

What have you learned about science over the course of this project? 
Science always comes with exciting surprises that do not always comply with our expectations, and it usually leaves more questions than answers. But it is gratifying to contribute, even in a small way, to the understanding of complex processes that can eventually be applied to solve difficult problems, such as the conservation of an endangered species.

Describe the significance of this research for the general scientific community in one sentence.
Adaptation to habitat change can happen, but perhaps not quickly or completely enough to overcome the negative effects of population reduction and fragmentation.

Describe the significance of this research for your scientific community in one sentence.
Landscape genomics analyses provide evidence of reduced gene flow in a fragmented habitat, leading to harmful effects on a critically endangered neotropical turtle, despite its possible adaptation to the new anthropogenically created environment.

Citation
Natalia Gallego‐García, Germán Forero‐Medina, Mario Vargas‐Ramírez, Susana Caballero, & Howard Bradley Shaffer. (2019). Landscape genomic signatures indicate reduced gene flow and forest‐associated adaptive divergence in an endangered neotropical turtle. Molecular Ecology, 28(11), 2757-2771. https://onlinelibrary.wiley.com/doi/10.1111/mec.15112

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