The Chinese giant salamander exemplifies the hidden extinction of cryptic species

Abstract

Overexploitation, habitat destruction, human-driven climate change and disease spread are resulting in the extinction of innumerable species, with amphibians being hit harder than most other groups [1]. Few species of amphibians are widespread, and those that are often represent complexes of multiple cryptic species. This is especially true for range-restricted salamanders [2]. Here, we used the widespread and critically endangered Chinese giant salamander (Andrias davidianus) to show how genetically uninformed management efforts can negatively affect species conservation. We find that this salamander consists of at least five species-level lineages. However, the extensive recent translocation of individuals between farms, where the vast majority of extant salamanders now live, has resulted in genetic homogenization. Mitochondrial DNA (mtDNA) haplotypes from northern China now predominate in farms. Unfortunately, hybrid offspring are being released back into the wild under well-intentioned, but misguided, conservation management. Our findings emphasize the necessity of genetic assessments for seemingly well-known, widespread species in conservation initiatives. Species serve as the primary unit for protection and management in conservation actions [3], so determining the taxonomic status of threatened species is a major concern, especially for amphibians. The level of threat to amphibians may be underestimated, and existing conservation strategies may be inadvertently harmful if conducted without genetic assessment.

Historical museum collections clarify the evolutionary history of cryptic species radiation in the world's largest amphibians

“…We analyzed samples from 21 historical Chinese giant salamander museum specimens with collection locality information obtained from China before 1922, and 20 tissue samples previously analyzed by Murphy et al () and Yan, Lü, et al () obtained in 1992 from giant salamanders with reported wild localities. Available samples represent four separate river drainages and nine provinces or equivalent administrative units and include the holotypes of Andrias davidianus and Megalobatrachus sligoi (Table ).…”

“…However, exploitation of giant salamanders increased in China from the late 1970s onwards, following the freeing of internal movement of people within China and the spread of southern Chinese migrants who had traditionally eaten the species; this led to trade and movement of animals across the country to supply a domestic luxury food market, and to development of a massive‐scale farming industry which has grown rapidly and expanded from southern Shaanxi Province across China since the early 2000s (Cunningham et al, ). The farming industry poses a huge threat to wild populations through continuing illegal harvesting of wild animals to stock farms, and serious risk of infectious disease transmission and genetic pollution associated with accidental escapes or deliberate “conservation” releases of farmed animals that have been moved around the country (Cunningham et al, ; Turvey et al, ; Yan, Lü, et al, ). The Chinese giant salamander is now listed as Critically Endangered by IUCN () and is recognized as a global conservation priority for maintaining evolutionary history (Isaac, Redding, Meredith, & Safi, ), because there are only two other living cryptobranchids (Japanese giant salamander, Andrias japonicus ; hellbender, Cryptobranchus alleganiensis ), which are both listed as Near Threatened by IUCN ().…”

“…Gray hatching indicates distribution of giant salamanders in Japan based on IUCN (). Inset, Chinese giant salamander ( Andrias davidianus ) found during 2013–2016 survey, assigned to clade B of Yan, Lü, et al (); see Turvey et al, …”

“…Giant salamanders are fully aquatic and occur in fast‐flowing tributaries within mountainous landscapes (Chen et al, ) across a series of different montane ecoregions that also represent areas of extensive local endemism (López‐Pujol, Zhang, Sun, Ying, & Ge, , ; Tang, Wang, Zheng, & Fang, ), and that can act as watersheds for multiple river drainages (e.g., Nanling mountains separate the Yangtze and Pearl drainages; Huangshan separates the Yangtze and Fujian‐Zhejiang hills drainages). Previous molecular phylogenetic analyses of giant salamander samples collected from across China (Murphy, Fu, Upton, Lema, & Zhao, ; Tao, Wang, Zheng, & Fang, ; Wang, Zhang, Xie, Wei, & Jiang, ; Yan, Lü, et al, ), which were investigated using isozymes, mitochondrial genes, microsatellites, or single nucleotide polymorphisms (SNPs), have identified genetically distinct local populations (e.g., a genetically distinct population from Huangshan; Murphy et al, ; Yan, Lü, et al, ). The most recent genetic study of wild‐caught and farmed Chinese giant salamander samples identified seven distinct lineages using mitochondrial genes (partial cytochrome b [cyt b ], COI , D‐loop) and nuclear SNPs (Yan, Lü, et al, ); some or all of these lineages were considered likely to represent cryptic species, thus revealing previously unsuspected levels of diversity within Chinese cryptobranchids.…”

“…The most recent genetic study of wild‐caught and farmed Chinese giant salamander samples identified seven distinct lineages using mitochondrial genes (partial cytochrome b [cyt b ], COI , D‐loop) and nuclear SNPs (Yan, Lü, et al, ); some or all of these lineages were considered likely to represent cryptic species, thus revealing previously unsuspected levels of diversity within Chinese cryptobranchids. However, these studies did not detail their findings against regional biogeographic patterns shown by other Chinese taxa and were also unable to consistently associate distinct clades with different landscapes, which they attributed to recent human movement of giant salamanders around China modifying local population structure and obscuring historical patterns of regional biogeographic differentiation (Murphy et al, ; Yan, Lü, et al, ). Indeed, genetic analysis of individuals found in the Yangtze and Pearl drainages during the 2013–2016 survey revealed these individuals all possessed a matriline characteristic of farmed individuals that originated from the Yellow River drainage, strongly suggesting they were farm escapes/releases (Turvey et al, ).…”