The importance of cryptic diversity in the conservation of wide-ranging species: The red-footed tortoise Chelonoidis carbonarius in Colombia.

Wide-ranging species are seldom considered conservation priorities, yet they have the potential to harbour genetically deeply differentiated units across environments or ecological barriers, including some that warrant taxonomic recognition. Documenting such cryptic genetic diversity is especially important for wide-ranging species that are in decline, as they may comprise a set of even more endangered lineages or species with small distributions. However, studies of wide-ranging species, particularly when they cross political borders, are extremely challenging. One approach to overcoming these challenges is to conduct detailed local analyses in combination with less detailed, range-wide studies. We used this approach with the red-footed tortoise (Chelonoidis carbonarius), a threatened species likely to contain cryptic diversity given its vast range and the distinctive ecoregions that it inhabits. Previous single-gene molecular studies indicated the presence of at least five lineages, two of which occur in different ecoregions separated by the Andes within Colombia. We used a comprehensive genomic analysis to test the hypothesis of cryptic diversity within the single jurisdiction of Colombia. We used a combination of restriction-site-associated DNA sequencing and environmental niche modelling to provide three independent lines of evidence that support the presence of important cryptic diversity that may deserve taxonomic recognition: allopatric reproductive isolation, local adaptation and ecological divergence. We also provide a fine-scale genetic map with the distribution of conservation units in Colombia. As we complete ongoing range-wide analyses and make taxonomic adjustments, we recommend that the two lineages in Colombia be treated as separate units for conservation purposes.

Las especies con distribuciones amplias rara vez son consideradas prioridades de conservación, sin embargo, tienen el potencial de albergar unidades genéticamente diferenciadas que en algunos casos justifican reconocimiento taxonómico. Documentar dicha diversidad genética críptica es especialmente importante para las especies de rangos amplios que ya están en peligro de extinción, pues pueden comprender un conjunto de linajes o especies aún más amenazadas y con distribuciones más pequeñas. Sin embargo, los estudios de especies de rangos amplios, particularmente cuando cruzan fronteras políticas, son extremadamente desafiantes. Un enfoque para superar estos desafíos es realizar análisis locales detallados en combinación con estudios en todo el rango de distribución menos detallados. Nosotros usamos este enfoque con la tortuga de patas rojas (Chelonoidis carbonarius), una especie amenazada que probablemente contiene diversidad genética críptica dada su amplia distribución y las distintas ecorregiones en las que habita. Estudios moleculares previos de un solo gen indicaron la presencia de al menos cinco linajes, dos de los cuales ocurren en diferentes ecorregiones separadas por los Andes en Colombia. En este estudio utilizamos una combinación de secuenciación de ADN asociada a sitios de restricción (RADseq) y modelamiento de nicho ecológico para proporcionar tres líneas independientes de evidencia que respaldan la presencia de diversidad críptica importante que puede merecer reconocimiento taxonómico: aislamiento reproductivo alopátrico, adaptación local y divergencia ecológica. También proporcionamos un mapa genético a escala fina con la distribución de unidades de conservación en Colombia. Mientras completamos análisis genómicos en todo el rango de distribución y hacemos ajustes taxonómicos, recomendamos que los dos linajes en Colombia se traten como unidades independientes para fines de conservación.

Are Genomic Updates of Well-Studied Species Worth the Investment for Conservation? A Case Study of the Critically Endangered Magdalena River Turtle.

As genomic-scale data sets become economically feasible for most organisms, a key question for conservation biology is whether the increased resolution offered by new genomic approaches justifies repeating earlier studies based on traditional markers, rather than investing those same time and monetary resources in less-known species. Genomic studies offer clear advantages when the objective is to identify adaptive loci that may be critical to conservation policy-makers. However, the answer is far less certain for the population and landscape studies based on neutral loci that dominate the conservation genetics research agenda. We used Restriction-site Associated DNA sequencing (RADseq) to revisit earlier molecular studies of the IUCN Critically Endangered Magdalena River turtle (Podocnemis lewyana), documenting the conservation insights gained by increasing the number of neutral markers by several orders of magnitude. Earlier research indicated that P. lewyana has the lowest genetic diversity known for any chelonian, and little or no population differentiation among independent rivers. In contrast, the RADseq data revealed discrete population structure with isolation-by-distance within river segments and identified precise population breaks clearly delineating management units. It also confirmed that the species does not have extremely low heterozygosity and that effective population sizes are probably sufficient to maintain long-term evolutionary potential. Contrary to earlier inferences from more limited population genetic markers, our genomic data suggest that management strategies should shift from active genetic rescue to more passive protection without extreme interventions. We conclude with a list of examples of conservation studies in other vertebrates indicating that for many systems a genomic update is worth the investment.

Landscape genomic signatures indicate reduced gene flow and forest-associated adaptive divergence in an endangered neotropical turtle.

Human-induced transformations of ecosystems usually result in fragmented populations subject to increased extinction risk. Fragmentation is also often associated with novel environmental heterogeneity, which in combination with restricted gene flow may increase the opportunity for local adaptation. To manage at-risk populations in these landscapes, it is important to understand how gene flow is changing, and how populations respond to habitat loss. We conducted a landscape genomics analysis using Restriction-site Associated DNA sequencing to investigate the evolutionary response of the critically endangered Dahl's Toad-headed turtle (Mesoclemmys dahli) to severe habitat modification. The species has lost almost all of its natural habitat in the southwestern part of its range and about 70% in the northeast. Based on least cost path analysis across different resistance surfaces for 3,211 SNPs, we found that the landscape matrix is restricting gene flow, causing the fragmentation of the species into at least six populations. Genome scans and allele-environment association analyses indicate that the population fragments in the deforested grasslands of the southwest are adaptively different from those in the more forested northeast. Populations in areas with no forest had low levels of adaptive genetic diversity and the fixation of ancestrally-polymorphic SNPs, consistent with directional selection in this novel environment. Our results suggest that this forest-stream specialist is adapting to pond-grassland conditions, but it is also suffering from negative consequences of habitat loss, including genetic erosion, isolation, small effective population sizes, and inbreeding. We recommend gene flow restoration via genetic rescue to counteract these threats, and provide guidance for this strategy.

Turtles and Tortoises Are in Trouble.

Turtles and tortoises (chelonians) have been integral components of global ecosystems for about 220 million years and have played important roles in human culture for at least 400,000 years. The chelonian shell is a remarkable evolutionary adaptation, facilitating success in terrestrial, freshwater and marine ecosystems. Today, more than half of the 360 living species and 482 total taxa (species and subspecies combined) are threatened with extinction. This places chelonians among the groups with the highest extinction risk of any sizeable vertebrate group. Turtle populations are declining rapidly due to habitat loss, consumption by humans for food and traditional medicines and collection for the international pet trade. Many taxa could become extinct in this century. Here, we examine survival threats to turtles and tortoises and discuss the interventions that will be needed to prevent widespread extinction in this group in coming decades.