Gut microbiomes play an essential role in host survival and local adaptation and thus can facilitate the invasion of host species. Biological invasions have been shown to be linked to the genetic properties of alien host species. It is thus plausible that the holobiont, the host, and its associated microbiome act as an entity to drive invasion success. The bighead carp and silver carp (bigheaded carps), invasive species that exhibit extensive hybridization in the Mississippi River Basin (MRB), provided a unique model to test the holobiont hypothesis of invasion. Here, we investigated the microbiomes of foreguts and hindguts in bigheaded carps and their reciprocal hybrids reared in aquaculture ponds using 16S amplicons and the associated gene prediction. We found an admixed pattern in the gut microbiome community in bigheaded carp hybrids. The hybrid gut microbiomes showed special characteristics such as relatively high alpha diversity in the foregut, an increasing dissimilarity between foreguts and hindguts, and a remarkable proportion of genes coding for putative enzymes related to their digestion of main food resources (Cyanobacteria, cellulose, and chitin). The pond-reared hybrids had advantageous features in genes coding for putative enzymes related to their diet. The above results collectively suggested that the gut microbiomes of hybrids could be beneficial to their local adaptation (e.g., food resource utilization), which might have facilitated their invasion in the MRB. The gut microbial findings, along with the intrinsic genomic features likely associated with life-history traits revealed in our recent study, provide preliminary evidence supporting the holobiont hypothesis of invasion.

Bighead carp (Hypophthalmichthys nobilis) and silver carp (Hypophthalmichthys molitrix), collectively called bigheaded carps, are invasive species in the Mississippi River Basin (MRB). Interspecific hybridization between bigheaded carps has been considered rare within their native rivers in China; however, it is prevalent in the MRB. We conducted de novo transcriptome analysis of pure and hybrid bigheaded carps and obtained 40,759 to 51,706 transcripts for pure, F1 hybrid, and backcross bigheaded carps. The search against protein databases resulted in 20,336-28,133 annotated transcripts (over 50% of the transcriptome) with over 13,000 transcripts mapped to 23 Gene Ontology biological processes and 127 KEGG metabolic pathways. More transcripts were detected in silver carp than in bighead carp; however, comparable numbers of transcripts were annotated. Transcriptomic variation detected between two F1 hybrids may indicate a potential loss of fitness in hybrids. The neighbor-joining distance tree constructed using over 2,500 one-to-one orthologous sequences suggests transcriptomes could be used to infer the history of introgression and hybridization. Moreover, we detected 24,792 candidate SNPs that can be used to identify different species. The transcriptomes, orthologous sequences, and candidate SNPs obtained in this study should provide further knowledge of interspecific hybridization and introgression.

The genetic paradox of biological invasions is complex and multifaceted. In particular, the relative role of disparate propagule sources and genetic adaptation through postintroduction hybridization has remained largely unexplored. To add resolution to this paradox, we investigate the genetic architecture responsible for the invasion of two invasive Asian carp species, bighead carp (Hypophthalmichthys nobilis) and silver carp (H. molitrix) (bigheaded carps) that experience extensive hybridization in the Mississippi River Basin (MRB). We sequenced the genomes of bighead and silver carps (~1.08G bp and ~1.15G bp, respectively) and their hybrids collected from the MRB. We found moderate-to-high heterozygosity in bighead (0.0021) and silver (0.0036) carps, detected significantly higher dN/dS ratios of single-copy orthologous genes in bigheaded carps versus 10 other species of fish, and identified genes in both species potentially associated with environmental adaptation and other invasion-related traits. Additionally, we observed a high genomic similarity (96.3% in all syntenic blocks) between bighead and silver carps and over 90% embryonic viability in their experimentally induced hybrids. Our results suggest intrinsic genomic features of bigheaded carps, likely associated with life history traits that presumably evolved within their native ranges, might have facilitated their initial establishment of invasion, whereas ex-situ interspecific hybridization between the carps might have promoted their range expansion. This study reveals an alternative mechanism that could resolve one of the genetic paradoxes in biological invasions and provides invaluable genomic resources for applied research involving bigheaded carps.