Genomic and Meiotic Changes Accompanying Polyploidization

Hybridization and polyploidy have been considered as significant evolutionary forces in adaptation and speciation, especially among plants. Interspecific gene flow generates novel genetic variants adaptable to different environments, but it is also a gene introgression mechanism in crops to increase their agronomical yield. An estimate of 9% of interspecific hybridization has been reported although the frequency varies among taxa. Homoploid hybrid speciation is rare compared to allopolyploidy. Chromosome doubling after hybridization is the result of cellular defects produced mainly during meiosis. Unreduced gametes, which are formed at an average frequency of 2.52% across species, are the result of altered spindle organization or orientation, disturbed kinetochore functioning, abnormal cytokinesis, or loss of any meiotic division. Meiotic changes and their genetic basis, leading to the cytological diploidization of allopolyploids, are just beginning to be understood especially in wheat. However, the nature and mode of action of homoeologous recombination suppressor genes are poorly understood in other allopolyploids. The merger of two independent genomes causes a deep modification of their architecture, gene expression, and molecular interactions leading to the phenotype. We provide an overview of genomic changes and transcriptomic modifications that particularly occur at the early stages of allopolyploid formation.

Independent evolution of intermediate bill widths in a seabird clade

Interspecific introgression can occur between species that evolve rapidly within an adaptive radiation. Pachyptila petrels differ in bill size and are characterised by incomplete reproductive isolation, leading to interspecific gene flow. Salvin’s prion (Pachyptila salvini), whose bill width is intermediate between broad-billed (P. vittata) and Antarctic (P. desolata) prions, evolved through homoploid hybrid speciation. MacGillivray’s prion (P. macgillivrayi), known from a single population on St Paul (Indian Ocean), has a bill width intermediate between salvini and vittata and could also be the product of interspecies introgression or hybrid speciation. Recently, another prion population phenotypically similar to macgillivrayi was discovered on Gough (Atlantic Ocean), where it breeds 3 months later than vittata. The similarity in bill width between the medium-billed birds on Gough and macgillivrayi suggest that they could be closely related. In this study, we used genetic and morphological data to infer the phylogenetic position and evolutionary history of P. macgillivrayi and the Gough medium-billed prion relative other Pachyptila taxa, to determine whether species with medium bill widths evolved through common ancestry or convergence. We found that Gough medium-billed prions belong to the same evolutionary lineage as macgillivrayi, representing a new population of MacGillivray’s prion that originated through a colonisation event from St Paul. We show that macgillivrayi’s medium bill width evolved through divergence (genetic drift) and independently from that of salvini, which evolved through hybridisation (gene flow). This represents the independent convergence towards a similarly medium-billed phenotype. The newly discovered MacGillivray’s prion population on Gough is of utmost conservation relevance, as the relict macgillivrayi population in the Indian Ocean is very small.

Extensive Interspecific Gene Flow Shaped Complex Evolutionary History and Underestimated Species Diversity in Rapidly Radiated Dolphins

Recently diverged taxa are often characterized by high rates of hybridization, which can complicate phylogenetic reconstruction. For this reason, the phylogenetic relationships and evolutionary history of dolphins are still not very well resolved; the question of whether the genera Tursiops and Stenella are monophyletic is especially controversial. Here, we performed re-sequencing of six dolphin genomes and combined them with eight previously published dolphin SRA datasets and six whole-genome datasets to investigate the phylogenetic relationships of dolphins and test the monophyly hypothesis of Tursiops and Stenella. Phylogenetic reconstruction with the maximum likelihood and Bayesian methods of concatenated loci, as well as with coalescence analyses of sliding window trees, produced a concordant and well-supported tree. Our studies support the non-monophyletic status of Tursiops and Stenella because the species referred these genera do not form exclusive monophyletic clades. This suggests that the current taxonomy of both genera might not reflect their evolutionary history and may underestimate their diversity. A four-taxon D-statistic (ABBA-BABA) test, five-taxon DFOIL test, and tree-based PhyloNet analyses all showed extensive gene flow across dolphin species, which could explain the instability in resolving phylogenetic relationship of oceanic dolphins with different and limited markers. This study could be a good case to demonstrate how genomic data can reveal complex speciation and phylogeny in rapidly radiating animal groups.

Genomic signals of admixture and reinforcement between two closely related species of European sepsid flies

Interspecific gene flow by hybridization may weaken species barriers and adaptive divergence, but can also initiate reinforcement of reproductive isolation trough natural and sexual selection. The extent of interspecific gene flow and its consequences for the initiation and maintenance of species barriers in natural systems remain poorly understood, however. To assess genome-wide patterns of gene flow between the two closely related European dung fly species Sepsis cynipsea and Sepsis neocynipsea (Diptera: Sepsidae), we tested for historical gene flow with the aid of ABBA-BABA test using whole-genome resequencing data from pooled DNA of male specimens originating from natural and laboratory populations. We contrasted genome-wide variation in DNA sequence differences between samples from sympatric populations of the two species in France and Switzerland with that of interspecific differences between pairs of samples involving allopatric populations from Estonia and Italy. In the French Cevennes, we detected a relative excess of DNA sequence identity, suggesting interspecific gene flow in sympatry. In contrast, at two sites in Switzerland, we observed a relative depletion of DNA sequence identity compatible with reinforcement of species boundaries in sympatry. Our results suggest that the species boundaries between S. cynipsea and S. neocynipsea in Europe depend on the eco-geographic context.

Evolutionary history of two rare endemic conifer species from the eastern Qinghai-Tibet Plateau

Background and Aims Understanding the population genetics and evolutionary history of endangered species is urgently needed in an era of accelerated biodiversity loss. This knowledge is most important for regions with high endemism that are ecologically vulnerable, such as the Qinghai-Tibet Plateau (QTP). Methods The genetic variation of 84 juniper trees from six populations of Juniperus microsperma and one population of Juniperus erectopatens, two narrow endemic junipers from the QTP that are sister to each other, was surveyed using RNA-seq data. Coalescent-based analyses were used to test speciation, migration, and demographic scenarios. Furthermore, positively selected and climate-associated genes were identified, and the genetic load was assessed for both species. Key Results Analyses of 149,052 single nucleotide polymorphisms showed that the two species are well-differentiated and monophyletic. They diverged around the late Pliocene, but interspecific gene flow continued until the Last Glacial Maximum. Demographic reconstruction by Stairway Plot detected two severe bottlenecks for J. microsperma and only one bottleneck for J. erectopatens. The identified positive selected genes and climate-associated genes revealed habitat adaptation of the two species. Furthermore, although J. microsperma had a much wider geographical distribution than J. erectopatens, the former possesses lower genetic diversity and a higher genetic load than the latter. Conclusions This study sheds light on the evolution of two endemic juniper species from the QTP and their responses to Quaternary climate fluctuations. Our findings emphasize the importance of speciation and demographic history reconstructions in the understanding of the current distribution pattern and genetic diversity of threatened species in mountainous regions.

Genome-Wide Evidence for Complex Hybridization and Demographic History in a Group of Cycas From China

Cycads represent one of the most ancestral living seed plants as well as one of the most threatened plant groups in the world. South China is a major center and potential origin of Cycas, the most rapidly diversified lineage of cycads. However, genomic-wide diversity of Cycas remains poorly understood due to the challenge of generating genomic markers associated with their inherent large genomes. Here, we perform a comprehensive conservation genomic study based on restriction-site associated DNA sequencing (RADseq) data in six representative species of Cycas in South China. Consistently low genetic diversity and strong genetic differentiation were detected across species. Both phylogenetic inference and genetic structure analysis via several methods revealed generally congruent groups among the six Cycas species. The analysis with ADMIXTURE showed low mixing of genetic composition among species, while individuals of C. dolichophylla exhibited substantial genetic admixture with C. bifida, C. changjiangensis, and C. balansae. Furthermore, the results from Treemix, f4-statistic, and ABBA-BABA test were generally consistent and revealed the complex patterns of interspecific gene flow. Relatively strong signals of hybridization were detected between C. dolichophylla and C. szechuanensis, and the ancestor of C. taiwaniana and C. changjiangensis. Distinct patterns of demographic history were inferred for these species by Stairway Plot, and our results suggested that both climate fluctuation and frequent geological activities during the late Pleistocene exerted deep impacts on the population dynamics of these species in South China. Finally, we explore the practical implications of our findings for the development of conservation strategies in Cycas. The present study demonstrates the efficiency of RADseq for conservation genomic studies on non-model species with large and complex genomes. Given the great significance of cycads as a radical transition in the evolution of plant biodiversity, our study provides important insights into the mechanisms of diversification in such recently radiated living fossil taxa.

Recurrent allopolyploidization events diversify eco-physiological traits in marsh orchids

Whole-genome duplication, in particular allopolyploidy, has shaped the evolution of angiosperms and other organisms. Structural reorganization of chromosomes and repatterning of gene expression is frequently observed in early generation allopolyploids, with potential ecological consequences. The relative contributions of environmental and intrinsic drivers to these changes are unknown. We show here that in marsh orchids (Dactylorhiza, Orchidaceae), recurrently-formed allopolyploids are characterized by distinct eco-physiologies matching their respective environments, providing us with an excellent study system to address this question. Here we integrate eco-physiological and transcriptomic comparative studies to reveal a complex suite of intertwined, pronounced differences between sibling allopolyploids. We show that Dactylorhiza majalis that is distributed in Central and Southern Europe favors meadows with mesic soils. Its sibling allopolyploid D. traunsteineri occurs in fens, characterized by soils depleted by macro- and micronutrients, mainly in previously glaciated European areas. We further uncover distinct features in their nutrient transport, leaf elemental chemistry, light-harvesting, photoprotection, and stomata activity, that appear all linked to their distinct ecologies, in particular soil chemistry differences at their native sites. Recurrent polyploidization hence enriches biodiversity through eco-physiological diversification, providing the opportunity for sibling allopolyploids to evolve as distinct evolutionary units, despite pervasive interspecific gene flow.Significance StatementWhole-genome duplication resulting in polyploidy has underpinned the evolution of flowering plants and other organisms, and is important for many crops. However, the ecological implications of polyploidy remain little understood. Here, we demonstrate that two sibling allopolyploid marsh orchid species prefer distinct habitats, and have evolved a suite of distinctive ecophysiological characters (e.g. nutrient transport, energy harvesting and photoprotection). We argue that the divergence of these characters in the nascent polyploids drove adaptation into distinct ecological niches (low nutrient fens versus meadows with mesic soils), generating ecological barriers that maintains distinct, independent lineages, even in the presence of interspecific gene flow.

Interspecific gene flow and vicariance in Northern African rear-edge white oak populations revealed by joint analysis of microsatellites and flanking sequences.

Rear-edge populations represent reservoirs of potentially unique genetic diversity but are particularly vulnerable to global changes. While continental-scale phylogeographic studies usually do not cover these populations, more focused local scale study of rear-edge populations should help better understand both past evolutionary history and its consequences for the persistence and conservation of these potentially unique populations. We studied molecular variation at 36 sequenced nuclear microsatellites in 11 rear-edge Quercus faginea and Q. canariensis populations across Algeria to shed light on taxonomic relationship, population past evolutionary history and recent demographic trajectory. We used descriptive approach and simulation-based inference to assess the information content and complementarity of linked microsatellite and flanking sequence variations. Genetic differentiation among populations classified into eight well-defined genetic clusters do not allow to unambiguously delineate two species. Instead, continuous level of genetic differentiation indicates interspecific gene flow or drift in isolation. Whereas the analysis of microsatellite variation allowed inferring recent interspecific gene flow, additional nucleotide variation in flanking sequences, by reducing homoplasy, pointed towards ancient interspecific gene flow followed by drift in isolation. The assessment of the weight of each polymorphism in the inference demonstrates the value of linked variation with contrasted mutational mechanisms and rates to refine historical demographic inference. Past population size decline inferred in some of these oak populations as well as low contemporary effective population size for most populations is a concern for the persistence of these populations of high evolutionary significance and conservation value.

Genomic methods reveal independent demographic histories despite strong morphological conservatism in fish species

Human overexploitation of natural resources has placed conservation and management as one of the most pressing challenges in modern societies, especially in regards to highly vulnerable marine ecosystems. In this context, cryptic species are particularly challenging to conserve because they are hard to distinguish based on morphology alone, and thus it is often unclear how many species coexist in sympatry, what are their phylogenetic relationships and their demographic history. We answer these questions using morphologically similar species of the genus Mugil that are sympatric in the largest coastal Marine Protected Area in the Tropical Southwestern Atlantic marine province. Using a sub-representation of the genome, we show that individuals are assigned to five highly differentiated genetic clusters that are coincident with five mitochondrial lineages, but discordant with morphological information, supporting the existence of five species with conserved morphology in this region. A lack of admixed individuals is consistent with strong genetic isolation between sympatric species, but the most likely species tree suggests that in one case speciation has occurred in the presence of interspecific gene flow. Patterns of genetic diversity within species suggest that effective population sizes differ up to two-fold, probably reflecting differences in the magnitude of population expansions since species formation. Together, our results show that strong morphologic conservatism in marine environments can lead to species that are difficult to distinguish morphologically but that are characterized by an independent evolutionary history, and thus that deserve species-specific management strategies.