Patterns of regulatory divergence and gene expression in hybrids are associated with molecular evolution in species undergoing gene flow

The extent to which hybridization disrupts a gene's pattern of expression likely governs its propensity for introgression, while its extent of molecular divergence can itself underlie such disruption. Together, these phenomena shape the landscape of sequence and transcriptional divergence across the genome as species diverge. To understand this process, we examine gene expression inheritance, regulatory and molecular divergences in the reproductive transcriptomes of species linked by gene flow. The fruit flies Anastrepha fraterculus and A. obliqua show evidence of gene flow despite clear evolutionary divergence and incomplete reproductive isolation. We find that their transcriptional patterns are a mosaic between those typically observed within and between allopatric species. Genes showing transgressive expression in hybrids or cis-regulatory divergence between species are associated with greater molecular divergence. This may reflect pleiotropic constraints that make them more resistant to gene flow or they may be more likely to experience divergent selection. However, while these highly divergent genes are likely to be important contributors to species differences, they are relatively rare. Instead, most differentially regulated genes, including those linked to reproduction, show high degrees of dominance in hybrids and trans-regulated divergence between species, suggesting widespread genetic compatibility that allowed for the identified introgression. These findings provide insights into how postzygotic isolating mechanisms might evolve in the presence of gene flow: regions showing cis-regulatory divergence or transgressive expression contribute to reproductive isolation, while regions with dominant expression and trans-regulatory divergence act as a buffer of hybrid breakdown, facilitating introgression, and leading to a genomic mosaic of expression and sequence divergence.

The Making of Calibration Sausage Exemplified by Recalibrating the Transcriptomic Timetree of Jawed Vertebrates

Molecular divergence dating has the potential to overcome the incompleteness of the fossil record in inferring when cladogenetic events (splits, divergences) happened, but needs to be calibrated by the fossil record. Ideally but unrealistically, this would require practitioners to be specialists in molecular evolution, in the phylogeny and the fossil record of all sampled taxa, and in the chronostratigraphy of the sites the fossils were found in. Paleontologists have therefore tried to help by publishing compendia of recommended calibrations, and molecular biologists unfamiliar with the fossil record have made heavy use of such works (in addition to using scattered primary sources and copying from each other). Using a recent example of a large node-dated timetree inferred from molecular data, I reevaluate all 30 calibrations in detail, present the current state of knowledge on them with its various uncertainties, rerun the dating analysis, and conclude that calibration dates cannot be taken from published compendia or other secondary or tertiary sources without risking strong distortions to the results, because all such sources become outdated faster than they are published: 50 of the (primary) sources I cite to constrain calibrations were published in 2019, half of the total of 280 after mid-2016, and 90% after mid-2005. It follows that the present work cannot serve as such a compendium either; in the slightly longer term, it can only highlight known and overlooked problems. Future authors will need to solve each of these problems anew through a thorough search of the primary paleobiological and chronostratigraphic literature on each calibration date every time they infer a new timetree, and that literature is not optimized for that task, but largely has other objectives.

Living in isolation for almost 40 years: molecular divergence of the 28S rDNA and COI sequences between French and Polish populations of the cave beetle Speonomus normandi hydrophilus (Jeannel, 1907)

The paper gives the results of the first studies on the molecular divergence between native and non-native populations of Speonomus normandi hydrophilus (Jeannel, 1907). This species is endemic to Massif Arize in the Central Pyrenees (France), and represents highly specialised organisms that live underground. In 1982, one hundred specimens of S. normandi hydrophilus had been experimentally introduced into the Dzwonnica Cave (Poland). Since then, a numerous population has developed in the Towarna-Dzwonnica cave system, and the neighbouring Cabanowa Cave. After almost 40 years of isolation between native and non-native populations, the genetic variations were examined using the COI and 28S rDNA genes. Analyses of the haplotypes of 28S showed one common haplogroup, which confirms the origin of the Polish group. The differentiation of haplotypes for the COI marker was high for both the French and Polish populations. Altogether 18 haplotypes of this marker have been detected, 12 in the French population and 9 in the Polish. However, only a portion of the haplotypes is shared between the native and introduced population.

Molecular Divergence in Flea Ctenocephalides Canis From West and Northwest of Iran

BackgroundFleas of the family Pulicidae are the most common ectoparasites infesting domestic livestock worldwide. The main aim of the present study was to demonstrate the degree of molecular divergence between Ctenocephalides canis fleas in the Western and Northwestern of Iran, based on nuclear and mitochondrial genes, including ITS1and ITS 2 and cytochrome c-oxidase 1 (cox1) mtDNA. MethodsA total of 918 C. canis fleas was collected. The obtained morphometric data and DNA sequencing results did not show significant differences between C. canis specimens from the different regions or hosts. However, there was a significant degree of molecular divergence among the ten populations based on nuclear markers.ResultsThe degree of molecular divergence between different isolates of C. canis based on ITS1and ITS 2 genes was 0.15% and 3.36%, respectively. But analysis of the sequencing results shows that there was no molecular divergence between the ten populations based on the Cox1 marker.ConclusionsStudy of internal transcribed spacer ITS1 and ITS2 of rDNA and the partial cox1 mtDNA gene showed that these fragments are useful tools for interspecific divergence rates, species-level differentiation and confirm the diagnosis of species C. canis.

Phylogenomic Resolution of Sea Spider Diversification through Integration of Multiple Data Classes

Despite significant advances in invertebrate phylogenomics over the past decade, the higher-level phylogeny of Pycnogonida (sea spiders) remains elusive. Due to the inaccessibility of some small-bodied lineages, few phylogenetic studies have sampled all sea spider families. Previous efforts based on a handful of genes have yielded unstable tree topologies. Here, we inferred the relationships of 89 sea spider species using targeted capture of the mitochondrial genome, 56 conserved exons, 101 ultraconserved elements, and 3 nuclear ribosomal genes. We inferred molecular divergence times by integrating morphological data for fossil species to calibrate 15 nodes in the arthropod tree of life. This integration of data classes resolved the basal topology of sea spiders with high support. The enigmatic family Austrodecidae was resolved as the sister group to the remaining Pycnogonida and the small-bodied family Rhynchothoracidae as the sister group of the robust-bodied family Pycnogonidae. Molecular divergence time estimation recovered a basal divergence of crown group sea spiders in the Ordovician. Comparison of diversification dynamics with other marine invertebrate taxa that originated in the Paleozoic suggests that sea spiders and some crustacean groups exhibit resilience to mass extinction episodes, relative to mollusk and echinoderm lineages.

Fossil Constraints on the Timescale of Parasitic Helminth Evolution

The fossil record of parasitic helminths is often stated to be severely limited. Many studies have therefore used host constraints to constrain molecular divergence time estimates of helminths. Here we review direct fossil evidence for several of these parasitic lineages belong to various phyla (Acanthocephala, Annelida, Arthropoda, Nematoda, Nematomorpha, Pentastomida, Platyhelminthes). Our compilation shows that the fossil record of soft-bodied helminths is patchy, but more diverse than commonly assumed. The fossil record provides evidence that ectoparasitic helminths (e.g., worm-like pentastomid arthropods) have been around since the early Paleozoic, while endoparasitic helminths (cestodes) arose at least during, or possibly even before the late Paleozoic. Nematode lineages parasitizing terrestrial plant and animal hosts have been in existence at least since the Devonian and Triassic, respectively. All major phyla (Acanthocephala, Annelida, Platyhelminthes. Nematoda, Nematomorpha) had evolved endoparasitic lineages at least since the Mesozoic. Interestingly, although parasitism is considered derived within Metazoa, the oldest evidence for Nematoda and Platyhelminthes includes body fossils of parasitic representatives. Furthermore, the oldest fossil evidence of these parasitic lineages often falls within molecular divergence time estimates based on host co-evolution suggesting the fossil record of helminths themselves might be just as good or at least complementary (and less circular in justification) to calibration based on host associations. Data also provide evidence for obvious host switches or extinctions, which cautions against models of pure co-divergence where use of host calibrations to constrain divergence time estimates may be considered.

Developmental and molecular characterization of novel staminodes in Aquilegia

Background and Aims The ranunculid model system Aquilegia is notable for the presence of a fifth type of floral organ, the staminode, which appears to be the result of sterilization and modification of the two innermost whorls of stamens. Previous studies have found that the genetic basis for the identity of this new organ is the result of sub- and neofunctionalization of floral organ identity gene paralogues; however, we do not know the extent of developmental and molecular divergence between stamens and staminodes. Methods We used histological techniques to describe the development of the Aquilegia coerulea ‘Origami’ staminode relative to the stamen filament. These results have been compared with four other Aquilegia species and the closely related genera Urophysa and Semiaquilegia. As a complement, RNA sequencing has been conducted at two developmental stages to investigate the molecular divergence of the stamen filaments and staminodes in A. coerulea ‘Origami’. Key Results Our developmental study has revealed novel features of staminode development, most notably a physical interaction along the lateral margin of adjacent organs that appears to mediate their adhesion. In addition, patterns of abaxial/adaxial differentiation are observed in staminodes but not stamen filaments, including asymmetric lignification of the adaxial epidermis in the staminodes. The comparative transcriptomics are consistent with the observed lignification of staminodes and indicate that stamen filaments are radialized due to overexpression of adaxial identity, while the staminodes are expanded due to the balanced presence of abaxial identity. Conclusions These findings suggest a model in which the novel staminode identity programme interacts with the abaxial/adaxial identity pathways to produce two whorls of laterally expanded organs that are highly differentiated along their abaxial/adaxial axis. While the ecological function of Aquilegia staminodes remains to be determined, these data are consistent with a role in protecting the early carpels from herbivory and/or pathogens.

Phylogenomic resolution of sea spider diversification through integration of multiple data classes

Despite significant advances in invertebrate phylogenomics over the past decade, the higher-level phylogeny of Pycnogonida (sea spiders) remains elusive. Due to the inaccessibility of some small-bodied lineages, few phylogenetic studies have sampled all sea spider families. Previous efforts based on a handful of genes have yielded unstable tree topologies. Here, we inferred the relationships of 89 sea spider species using targeted capture of the mitochondrial genome, 56 conserved exons, 101 ultraconserved elements, and three nuclear ribosomal genes. We inferred molecular divergence times by integrating morphological data for fossil species to calibrate 15 nodes in the arthropod tree of life. This integration of data classes resolved the basal topology of sea spiders with high support. The enigmatic family Austrodecidae was resolved as the sister group to the remaining Pycnogonida and the small-bodied family Rhynchothoracidae as the sister group of the robust-bodied family Pycnogonidae. Molecular divergence time estimation recovered a basal divergence of crown group sea spiders in the Ordovician. Comparison of diversification dynamics with other marine invertebrate taxa that originated in the Paleozoic suggests that sea spiders and some crustacean groups exhibit resilience to mass extinction episodes, relative to mollusk and echinoderm lineages.