Researchers Reveal Genetic Mechanisms Underlying Invasion Success of Carassius auratus in a High-altitude Environment

The fish diversity of the Qinghai-Tibet Plateau (QTP) is very sensitive and vulnerable to biological invasion due to the fragile ecosystem and unique fish fauna. One of the most widespread invasive species in the QTP is Carassius auratus which represents a remarkable species complex containing individuals with different ploidy levels in natural waters. They have different reproduction modes, with diploids exhibiting sexual reproduction and triploids exhibiting unisexual gynogenesis. If both sexual diploids and unisexual triploids have been included in invasive populations on the QTP, this raises an interesting possibility to compare the genetic responses of the two forms. 

Based on our market survey, C. auratus in Tibet is directly imported from the aquatic product markets in Ningxia and Sichuan Provinces. In addition, C. auratus in Ningxia was also imported from the central and eastern regions along the Yangtze River and Huai River. Hence, invasive populations of C. auratus in Tibet came from diverse sources which may be genetically distinct. Previous studies of multiple invasive species have shown that multiple introductions from the same or distinct source populations may have prevented or even reversed loss of genetic diversity within the invasive range. However, given the extreme environmental conditions on the QTP, this begs the question to which extent genetic diversity of C. auratus has been shaped by the extreme environments that it has been transplanted into during multiple introductions. 

Recently, a research group led by Prof. CHEN Yifeng from the Institute of Hydrobiology (IHB) of the Chinese Academy of Sciences analyzed the whole-genome resequencing data of 151 C. auratus individuals from two invasive and 11 native populations and found different patterns of genomic responses between diploid and triploid populations during their invasion of Tibet. This study was published in Molecular Ecology. 

Based on 16,888,283 SNPs identified for diploids, the researchers found two clear genetic clusters which consisted of invasive and native individuals, respectively. The genetic cluster of native individuals split into three subclusters which followed a pattern of geographical separation. Highly significant genetic differentiation was detected between the invasive population and three genetic subclusters from the native range. Although invasive individuals had a relative higher diversity (π) than source individuals at the population level, their individual genetic diversity (genome-wide observed heterozygosity) were significantly lower (21.4%) than those of source individuals. 

Based on 17,954,020 SNPs identified for triploids, the researchers found that the pattern of population structure was not related to the geographical origin and the invasive individuals were not separate from natives. No significant genetic differentiation was observed between invasive populations and native populations. Invasive individuals also had a slightly higher π value than source individuals at the population level, their individual genetic diversity were comparable to those of the native individuals. 

Recent inbreeding, founder events and selective sweeps which detected in invasive diploids were the main factors causing changes of genetic diversity and population structure. However, invasive triploids experienced no change in genetic diversity owing to their reproduction mode of gynogenesis that precludes inbreeding and founder effects and may make them more powerful invaders. 

These findings reveal the genetic mechanisms underlying the invasion success of C. auratus in a high-altitude environment, and thereby providing theoretical foundations for the prevention and control of invasive fishes on the Qinghai-Tibet Plateau and enhancing our understanding of the rapid evolutionary adaptation of the species with different reproductive modes in a new environment.