Striking habitat reduction, decreased genetic diversity, and imperilled conservation of natural populations of Terrapenecoahuila

Abstract

Long‐term evolutionary history and demographic processes shape current patterns of genetic variation in natural populations. Genetic diversity is of prime importance for the long‐term survival of species, especially those threatened or endangered, which can be lost in a few generations and can take hundreds to recover. Notably, turtles are among the most endangered vertebrate taxa in the world. The Coahuilan box turtle Terrapene coahuila is the only aquatic species within the genus, microendemic to the desert‐spring ecosystem of the Cuatrociénegas Basin (CCB). The CCB has experienced significant habitat changes during recent decades, fragmenting otherwise interconnected wetlands systems. We aimed to perform a detailed evaluation of the evolutionary and genetic patterns of T. coahuila, both historical and contemporary, linked to the biogeography of the CCB and processes governing the species distribution. We assessed the contributions of historical and contemporary population demographic processes to genetic diversity and structure, by using two mitochondrial DNA genes (cytochrome b and d‐loop), one nuclear gene (GAPD), and 12 nuclear microsatellite loci. We comprehensively analysed these data to address historical patterns of demography, migration, genetic diversity, and times of divergence across the valley for T. coahuila. We also evaluated recent patterns of genetic variation and structure, inbreeding, bottleneck signals, and effective population size. Our results dated the time to the most recent common ancestor for T. coahuila in the CCB at c. 10.1 million years ago, with highest diversification during the Holocene. Structure consistently comprised two genetic clusters, Cuatrociénegas East and Cuatrociénegas West on either side of the main historical barrier, the Sierra San Marcos. Demographic results supported a divergence between western and eastern populations from 47,500 to 110,950 years ago, and colonisation of the southernmost Cuatrociénegas West distribution (Churince) 28,500–66,500 years ago, which experienced a recent bottleneck. All populations showed low values of haplotype and nuclear genetic diversity, migration, effective population size, and relatedness; significant inbreeding and bottleneck signals were also identified within genetic clusters. In accordance with the biogeographic history of the basin, our results show that T. coahuila’s diversification across the Cuatrociénegas valley continued throughout the Pleistocene, peaking during the Holocene, when the valley started to gradually dry. As predicted, T. coahuila exhibited an overall, long‐term, and probably continuing decrement in genetic variation, increased genetic differentiation, and low population sizes, as a consequence of contemporary habitat loss and fragmentation across the CCB. Changes in species demography and population connectivity have the potential to permanently alter the genetic patterns of freshwater species. Hence, given its restricted distribution, high habitat specificity and habitat loss, Terrapene coahui...

Complex genetic patterns and distribution limits mediated by native congeners of the worldwide invasive red‐eared slider turtle

“…Very little is known about the biology and ecology of T. taylori, but there is no doubt that they have rather low population sizes, probably due to their endemism but also to the contemporary habitat loss and fragmentation across the CCB, as recently described for T. coahuila (Cortés-Rodríguez et al, 2021). Accordingly, T. taylori are highly diverged from other Trachemys species and they present the lowest genetic diversity.…”

“…Trachemys taylori , microendemic to the desert‐spring ecosystem of the Cuatrociénegas Basin (CCB), Coahuila, Mexico, is only found in permanent and seasonal wetlands across the CCB valley (Seidel, 2002a). The CCB wetland has shrunk 90% in the last 60 years, mainly as a result of water extraction and channelling through a complex system of artificial courses and canals, significantly reducing the natural distribution of many species, including other endemic turtles ( Terrapene coahuila , Apalone atra ; Cortés‐Rodríguez et al, 2021). Very little is known about the biology and ecology of T .…”

“…taylori , but there is no doubt that they have rather low population sizes, probably due to their endemism but also to the contemporary habitat loss and fragmentation across the CCB, as recently described for T . coahuila (Cortés‐Rodríguez et al, 2021). Accordingly, T .…”

Complex genetic patterns and distribution limits mediated by native congeners of the worldwide invasive red-eared slider turtle

“…Trachemys taylori, microendemic to the desert-spring ecosystem of the Cuatrociénegas Basin (CCB), Coahuila, Mexico, is only found in permanent and seasonal wetlands across the CCB valley (Siedel, 2002a). The CCB wetland has shrunk 90% in the last 60 years, mainly as a result of water extraction and channeling through a complex system of artificial courses and canals, significantly reducing the natural distribution of many species, including other endemic turtles (Terrapene coahuila, Apalone atra; Cortés-Rodríguez et al, 2021). Very little is known about the biology and ecology of T. taylori, but there is no doubt that they have rather low population sizes, likely due to their endemism but also to the contemporary habitat loss and fragmentation across the CCB, as recently described for T. coahuila (Cortés-Rodríguez et al, 2021).…”

“…The CCB wetland has shrunk 90% in the last 60 years, mainly as a result of water extraction and channeling through a complex system of artificial courses and canals, significantly reducing the natural distribution of many species, including other endemic turtles (Terrapene coahuila, Apalone atra; Cortés-Rodríguez et al, 2021). Very little is known about the biology and ecology of T. taylori, but there is no doubt that they have rather low population sizes, likely due to their endemism but also to the contemporary habitat loss and fragmentation across the CCB, as recently described for T. coahuila (Cortés-Rodríguez et al, 2021). Accordingly, T. taylori are highly diverged from other Trachemys species and they present the lowest genetic diversity.…”