Population genetics reveals cryptic lineages and ongoing hybridization in a declining migratory fish species complex

Deciphering the effects of historical and recent demographic processes responsible for the spatial patterns of genetic diversity and structure is a key objective in evolutionary and conservation biology. Using genetic analyses, we investigated the demographic history, the contemporary genetic diversity and structure, and the occurrence of hybridization and introgression, of two species of anadromous fish with contrasted life history strategies and which have undergone recent demographic declines, the allis shad (Alosa alosa) and the twaite shad (Alosa fallax). We genotyped 706 individuals from 20 rivers and 5 sites at sea in Southern Europe at microsatellite markers. Genetic structure between populations was lower for the nearly semelparous species allis shad that disperse stronger distance compared to the iteroparous species, twaite shad. Individuals caught at sea were assigned at the river level for twaite shad and at the region level for allis shad. Using an approximate Bayesian computation framework, we inferred that the most likely long term historical divergence scenario between both species implicated historical separation followed by secondary contact accompanied by strong population size decline. Accordingly, we found evidence of contemporary hybridization and introgression between both species. Besides, our results support the existence of cryptic species in the Mediterranean sea. Overall, our results shed light on the interplay between historical and recent demographic processes and life history strategies in shaping population genetic diversity and structure of closely related species. The recent demographic decline of these species’ populations and their hybridization should be carefully considered while implementing conservation programs.

Hybridization and introgression are prevalent in Southern European Erysimum (Brassicaceae) species

Background and Aims: Hybridization is a common and important force in plant evolution. One of its outcomes is introgression - the transfer of small genomic regions from one taxon to another by hybridization and repeated backcrossing. This process is believed to be common in glacial refugia, where range expansions and contractions can lead to cycles of sympatry and isolation, creating conditions for extensive hybridization and introgression. Polyploidization is another genome-wide process with a major influence on plant evolution. Both hybridization and polyploidization can have complex effects on plant evolution. However, these effects are often difficult to understand in recently evolved species complexes. Methods: We combined flow cytometry, transcriptomic and genomic analyses, and pollen-tube growth assays to investigate the consequences of polyploidization, hybridization, and introgression on the recent evolution of several Erysimum (Brassicaceae) species from the South of the Iberian Peninsula, a well-known glacial refugium. This species complex differentiated in the last 2Myr, and its evolution has been hypothesized to be determined mainly by polyploidization, interspecific hybridization, and introgression. Key Results: Our results support a scenario of widespread hybridization involving both extant and ghost taxa. Several taxa studied here, most notably those with purple corollas, are polyploids, likely of allopolyploid origin. Moreover, hybridization in this group might be an ongoing phenomenon, as prezygotic barriers appeared weak in many cases. Conclusions: The evolution of Erysimum spp. has been determined by hybridization to a large extent. The adaptive value of such genomic exchanges remains unclear, but our results indicate the importance of hybridization for plant diversification across evolutionary scales.

Plastome Characterization and Phylogenomic Analysis Yield New Insights into the Evolutionary Relationships among the Species of the Subgenus Bryocles (Hosta; Asparagaceae) in East Asia

The genus Hosta, which has a native distribution in temperate East Asia and a number of species ranging from 23 to 40, represents a taxonomically important and ornamentally popular plant. Despite its taxonomic and horticultural importance, the genus Hosta has remained taxonomically challenging owing to insufficient diagnostic features, continuous morphological variation, and the process of hybridization and introgression, making species circumscription and phylogenetic inference difficult. In this study, we sequenced 11 accessions of Hosta plastomes, including members of three geographically defined subgenera, Hosta, Bryocles, and Giboshi, determined the characteristics of plastomes, and inferred their phylogenetic relationships. We found highly conserved plastomes among the three subgenera, identified several mutation hotspots that can be used as barcodes, and revealed the patterns of codon usage bias and RNA editing sites. Five positively selected plastome genes (rbcL, rpoB, rpoC2, rpl16, and rpl20) were identified. Phylogenetic analysis suggested (1) the earliest divergence of subg. Hosta, (2) non-monophyly of subg. Bryocles and its two sections (Lamellatae and Stoloniferae), (3) a sister relationship between H. sieboldiana (subg. Giboshi) and H. ventricosa (subg. Bryocles), and (4) reciprocally monophyletic and divergent lineages of H. capitata in Korea and Japan, requiring further studies of their taxonomic distinction.

Phylogenomic assessment of the role of hybridization and introgression in trait evolution

Trait evolution among a set of species—a central theme in evolutionary biology—has long been understood and analyzed with respect to a species tree. However, the field of phylogenomics, which has been propelled by advances in sequencing technologies, has ushered in the era of species/gene tree incongruence and, consequently, a more nuanced understanding of trait evolution. For a trait whose states are incongruent with the branching patterns in the species tree, the same state could have arisen independently in different species (homoplasy) or followed the branching patterns of gene trees, incongruent with the species tree (hemiplasy). Another evolutionary process whose extent and significance are better revealed by phylogenomic studies is gene flow between different species. In this work, we present a phylogenomic method for assessing the role of hybridization and introgression in the evolution of polymorphic or monomorphic binary traits. We apply the method to simulated evolutionary scenarios to demonstrate the interplay between the parameters of the evolutionary history and the role of introgression in a binary trait’s evolution (which we call xenoplasy). Very importantly, we demonstrate, including on a biological data set, that inferring a species tree and using it for trait evolution analysis in the presence of gene flow could lead to misleading hypotheses about trait evolution.

Introgression shapes fruit color convergence in invasive Galápagos tomato

Invasive species represent one of the foremost risks to global biodiversity. Here, we use population genomics to evaluate the history and consequences of an invasion of wild tomato-Solanum pimpinellifolium-onto the Galápagos islands from continental South America. Using >300 archipelago and mainland collections, we infer this invasion was recent and largely the result of a single event from central Ecuador. Patterns of ancestry within the genomes of invasive plants also reveal post-colonization hybridization and introgression between S. pimpinellifolium and the closely related Galapagos endemic Solanum cheesmaniae. Of admixed invasive individuals, those that carry endemic alleles at one of two different carotenoid biosynthesis loci also have orange fruits-characteristic of the endemic species-instead of typical red S. pimpinellifolium fruits. We infer that introgression of two independent fruit color loci explains this observed trait convergence, suggesting that selection has favored repeated transitions of red to orange fruits on the Galapagos.

Hybridization and introgression in sympatric and allopatric populations of four oak species

Background Hybridization and introgression are vital sources of novel genetic variation driving diversification during reticulated evolution. Quercus is an important model clade, having extraordinary diverse and abundant members in the Northern hemisphere, that are used to studying the introgression of species boundaries and adaptive processes. China is the second-largest distribution center of Quercus, but there are limited studies on introgressive hybridization. Results Here, we screened 17 co-dominant nuclear microsatellite markers to investigate the hybridization and introgression of four oaks (Quercus acutissima, Quercus variabilis, Quercus fabri, and Quercus serrata) in 10 populations. We identified 361 alleles in the four-oak species across 17 loci, and all loci were characterized by high genetic variability (HE = 0.844–0.944) and moderate differentiation (FST = 0.037–0.156) levels. A population differentiation analysis revealed the following: allopatric homologous (FST = 0.064) < sympatric heterogeneous (FST = 0.071) < allopatric heterogeneous (FST = 0.084). A Bayesian admixture analysis determined four types of hybrids (Q. acutissima × Q. variabilis, Q. fabri × Q. serrata, Q. acutissima × Q. fabri, and Q. acutissima × Q. variabilis × Q. fabri) and their asymmetric introgression. Our results revealed that interspecific hybridization is commonly observed within the section Quercus, with members having tendency to hybridize. Conclusions Our study determined the basic hybridization and introgression states among the studied four oak species and extended our understanding of the evolutionary role of hybridization. The results provide useful theoretical data for formulating conservation strategies.

Hybridization in Selected Species and Genera of Diaptomid Copepods in China

To better understand the fauna of freshwater calanoid copepods of China, including the occurrence of intra- and intergeneric hybridization, we studied five species, distributed across the whole of China or in South China. We sequenced a mitochondrial (COI) and the nuclear ribosome 18S operon (ITS) to reconstruct the phylogenetic trees by using a Bayesian and maximum likelihood (ML) approach with 161 individuals. The phylogeny tree revealed five clades and two geographically separated subclades in both S. ferus and P. tunguidus. We found, for the first time, that the hybrid specimens occurred in Diaptomidae, but low hybridization suggested effective barriers to hybridization and introgression. One hypothesis, that hybridization is recent and was initiated by invasions via canals built between the Yangtze and Pearl rivers c. 2000 years ago, is not supported by K2P genetic distances of the order of 20%. Furthermore, COI analysis of different populations of S. ferus and P. tunguidus revealed two geographical clades in each species, with genetic distances commensurate with cryptic speciation. Both clades occupy subranges maintained without visible barriers to mixis.

Population Transcriptomics Reveals Gene Flow and Introgression Between Two Non-sister Alpine Gentians

Distributional shifts driven by Quaternary climatic oscillations have been suggested to cause interspecific hybridization and introgression. In this study, we aimed to test this hypothesis by using population transcriptomes and coalescent modeling of two alpine none-sister gentians. Previous studies suggested that historical hybridizations occurred between Gentiana siphonantha and G. straminea in the high-altitude Qinghai-Tibet Plateau although both species are not sister to each other with the most recent divergence. In the present study, we sequenced transcriptomes of 33 individuals from multiple populations of G. siphonantha and G. straminea. The two species are well delimited by nuclear genomic SNPs while phylogenetic analyses of plastomes clustered one G. straminea individual into the G. siphonantha group. Further population structure analyses of the nuclear SNPs suggested that two populations of G. siphonantha were admixed with around 15% ancestry from G. straminea. These analyses suggested genetic introgressions from G. straminea to G. siphonantha. In addition, our coalescent-based modeling results revealed that gene flow occurred between the two species since Last Glacier Maximum after their initial divergence, which might have leaded to the observed introgressions. Our results underscore the significance of transcriptome population data in determining timescale of interspecific gene flow and direction of the resulting introgression.