Loss of plastid developmental genes coincides with a reversion to monoplastidy in hornworts

The first plastid evolved from an endosymbiotic cyanobacterium in the common ancestor of the Archaeplastida. The transformative steps from cyanobacterium to organelle included the transfer of control over developmental processes; a necessity for the host to orchestrate, for example, the fission of the organelle. The plastids of almost all embryophytes divide independent from nuclear division, leading to cells housing multiple plastids. Hornworts, however, are monoplastidic (or near-monoplastidic) and their photosynthetic organelles are a curious exception among embryophytes for reasons such as the occasional presence of pyrenoids. Here we screened genomic and transcriptomic data of eleven hornworts for components of plastid developmental pathways. We find intriguing differences among hornworts and specifically highlight that pathway components involved in regulating plastid development and biogenesis were differentially lost in this group of bryophytes. In combination with ancestral state reconstruction, our data suggest that hornworts have reverted back to a monoplastidic phenotype due to the combined loss of two plastid division-associated genes: ARC3 and FtsZ2.

Substantial rearrangements, single nucleotide frameshift deletion and low diversity in mitogenome of Wolbachia-infected strepsipteran endoparasitoid in comparison to its tephritid hosts

Insect mitogenome organisation is highly conserved, yet, some insects, especially with parasitic life cycles, have rearranged mitogenomes. Furthermore, intraspecific mitochondrial diversity can be reduced by fitness-affecting bacterial endosymbionts like Wolbachia due to their maternal coinheritance with mitochondria. We have sequenced mitogenomes of the Wolbachia-infected endoparasitoid Dipterophagus daci (Strepsiptera: Halictophagidae) and four of its 22 known tephritid fruit fly host species using total genomic extracts of parasitised flies collected across > 700 km in Australia. This halictophagid mitogenome revealed extensive rearrangements relative to the four fly mitogenomes which exhibited the ancestral insect mitogenome pattern. Compared to the only four available other strepsipteran mitogenomes, the D. daci mitogenome had additional transpositions of one rRNA and two tRNA genes, and a single nucleotide frameshift deletion in nad5 requiring translational frameshifting or, alternatively, resulting in a large protein truncation. Dipterophagus daci displays an almost completely endoparasitic life cycle when compared to Strepsiptera that have maintained the ancestral state of free-living adults. Our results support the hypothesis that the transition to extreme endoparasitism evolved together with increased levels of mitogenome changes. Furthermore, intraspecific mitogenome diversity was substantially smaller in D. daci than the parasitised flies suggesting Wolbachia reduced mitochondrial diversity because of a role in D. daci fitness.

Transcriptome-based phylogeny of the semi-aquatic bugs (Hemiptera: Heteroptera: Gerromorpha) reveals patterns of lineage expansion in a series of new adaptive zones

Key innovations enable access to new adaptive zones and are often linked to increased species diversification. As such, they have attracted much attention, yet their concrete consequences on the subsequent evolutionary trajectory and diversification of the bearing lineages remain unclear. The monophyletic group of water striders and relatives (Hemiptera: Heteroptera: Gerromorpha) represent a group of insects that transited to live on the water-air interface and diversified to occupy ponds, puddles, streams, mangroves and even oceans. This lineage offers an excellent model to study the patterns and processes underlying species diversification following the conquest of new adaptive zones. However, such studies require a reliable and comprehensive phylogeny of the infraorder. Based on whole transcriptomic datasets of 97 species and fossil records, we reconstructed a new phylogeny of the Gerromorpha that resolved inconsistencies and uncovered strong support for previously unknown relationships between some important taxa. We then used this phylogeny to reconstruct the ancestral state of a set of adaptations associated with water surface invasion (fluid locomotion, dispersal and transition to saline waters) and sexual dimorphism. Our results uncovered important patterns and dynamics of phenotypic evolution revealing how the initial event of water surface invasion enabled multiple subsequent transitions to new adaptive zones, representing distinct niches of water surfaces, and further diversification of the group. This phylogeny and the associated transcriptomic datasets constitute highly valuable resources, making Gerromorpha an attractive model lineage to study phenotypic evolution.

Maternal investment evolves with larger body size and higher diversification rate in sharks and rays

Across vertebrates, live-bearing has evolved at least 150 times from the ancestral state of egg-laying into a diverse array of forms and degrees of prepartum maternal investment. A key question is how this diversity of reproductive modes arose and whether reproductive diversification underlies species diversification? To test these questions, we evaluate the most basal jawed vertebrates, Chondrichthyans, which have one of the greatest ranges of reproductive and ecological diversity among vertebrates. We reconstructed the sequence of reproductive mode evolution across a time-calibrated molecular phylogeny of 610 chondrichthyans. We find that egg-laying is ancestral, and that live-bearing evolved at least seven times. Matrotrophy (i.e. additional maternal contributions) evolved at least 15 times, with evidence of one reversal. In sharks, transitions to live-bearing and matrotrophy are more prevalent in larger-bodied species in the tropics. Further, the evolution of live-bearing is associated with a near-doubling of the diversification rate, but, there is only a small increase in diversification associated with the appearance of matrotrophy. The chondrichthyan diversification and radiation, particularly throughout the shallow tropical shelf seas and oceanic pelagic habitats, appears to be associated with the evolution of live-bearing and the proliferation of a wide range of maternal investment in their developing offspring.

Dynamic evolution of small signaling peptide compensation in plant stem cell control

Gene duplications are a hallmark of plant genome evolution and a foundation for genetic interactions that shape phenotypic diversity. Compensation is a major form of paralog interaction, but how compensation relationships change as allelic variation accumulates is unknown. Here, we leveraged genomics and genome editing across the Solanaceae family to capture the evolution of compensating paralogs. Mutations in the stem cell regulator CLV3 cause floral organs to overproliferate in many plants. In tomato, this phenotype is partially suppressed by transcriptional upregulation of a closely related paralog. Tobacco lost this paralog, resulting in no compensation and extreme clv3 phenotypes. Strikingly, the paralogs of petunia and groundcherry nearly completely suppress clv3, indicating a potent ancestral state of compensation. Cross-species transgenic complementation analyses show this potent compensation partially degenerated in tomato due to a single amino acid change in the paralog and cis-regulatory variation that limits its transcriptional upregulation. Our findings show how genetic interactions are remodeled following duplications, and suggest that dynamic paralog evolution is widespread over short time scales and impacts phenotypic variation from natural and engineered mutations.

Tracing the evolution of bioluminescent light organs across the deep-sea shrimp family Sergestidae using a genomic skimming and phylogenetic approach

Deep-sea shrimp of the family Sergestidae Dana, 1852 provide a unique system for studying the evolution of bioluminescence. Most species within the family possess autogenic bioluminescent photophores in one of three distinct forms: lensed photophores; non-lensed photophores; or internal organs of Pesta. This morphological diversity across the Sergestidae has resulted in recent major taxonomic revisions, dividing the two major genera (Sergia Stimpson, 1860 and Sergestes Milne Edwards, 1830) into 15. The present study capitalises on molecular data to construct an updated genus-level phylogeny of sergestid shrimp. DNA was successfully extracted from ~87 individuals belonging to 13 of the 15 newly proposed genera. A ‘genome skimming’ approach was implemented, allowing the capture of mitochondrial genomic data across 19 sergestid species. Additional individuals have been incorporated into the phylogeny through Sanger sequencing of both nuclear (H3 and NAK) and mitochondrial (16S and COI) genes. The resulting molecular phylogeny is compared with previous morphological trees with specific attention to genus-level relationships. The -sergestes group was rendered non-monophyletic and the -sergia group was recovered as monophyletic. Ancestral state reconstructions of light organ type indicate that organs of Pesta is the ancestral state for the family. Non-lensed photophores evolved once across the -sergia group, but were later lost in the deepest living genus, Sergia. Lensed photophores also evolved once within the genera Prehensilosergia Vereshchaka, Olesen & Lunina, 2014, Lucensosergia Vereshchaka, Olesen & Lunina, 2014 and Challengerosergia Vereshchaka, Olesen & Lunina, 2014. These findings identify preliminary patterns across light organ type and species’ depth distributions; however, future research that incorporates finer-scale depth data and more species is needed to confirm our findings.

Towards a global perspective for Salvia L: Phylogeny, diversification, and floral evolution

Premise of this study: Salvia is the most species-rich genus in Lamiaceae, encompassing approximately 1000 species distributed all over the world. We sought a new evolutionary perspective for Salvia by employing macroevolutionary analyses to address the tempo and mode of diversification. To study the association of floral traits with speciation and extinction, we modeled and explored the evolution of corolla length and the lever-mechanism pollination system across our Salvia phylogeny. Methods: We reconstructed a multigene phylogeny for 366 species of Salvia in the broad sense including all major recognized lineages and numerous species from Iran, a region previously overlooked in studies of the genus. Our phylogenetic data in combination with divergence time estimates were used to examine the evolution of corolla length, woody vs. herbaceous habit, and presence vs. absence of a lever mechanism. We investigated the timing and dependence of Salvia diversification related to corolla length evolution through a disparity test and BAMM analysis. A HiSSE model was used to evaluate the dependency of diversification on the lever-mechanism pollination system in Salvia. Key Results: Based on recent investigations and classifications, Salvia is monophyletic and comprises ~1000 species. Our inclusion, for the first time, of a comprehensive sampling for Iranian species of Salvia provides higher phylogenetic resolution for southwestern Asian species than obtained in previous studies. A medium corolla length (15-18mm) was reconstructed as the ancestral state for Salvia with multiple shifts to shorter and longer corollas. Macroevolutionary model analyses indicate that corolla length disparity is high throughout Salvia evolution, significantly different from expectations under a Brownian motion model during the last 28 million years of evolution. Our analyses show evidence of a higher diversification rate of corolla length for some Andean species of Salvia compared to other members of the genus. Based on our tests of diversification models, we reject the hypothesis of a direct effect of the lever mechanism on Salvia diversification. Conclusions: Using a broader species sampling than previous studies, we obtained a well-resolved phylogeny for southwest Asian species of Salvia. Corolla length is an adaptive trait throughout the Salvia phylogeny with a higher rate of diversification in the South American clade. Our results suggest caution in considering the lever-mechanism pollination system as one of the main drivers of speciation in Salvia.

Sensory convergence in the world s largest cavefish diversification: patterns of neuromast evolution, distribution and associated behaviour in Sinocyclocheilus

Sinocyclocheilus represents the largest freshwater cavefish genus in the world. This emerging model system is endemic to the southern Chinese karstic landscape, and demonstrates multiple adaptations for life in caves (troglomorphism), with eye-degeneration being the most pronounced. The less-apparent lateral line system, which is often expanded in cave-dwellers, has been studied in other cavefish systems, but never in the context of this diversification. Here we investigated the distribution and evolution of cephalic neuromasts in 26 Sinocyclocheilus species. We used live-staining and behavioural assays, and interpreted results in a phylogenetic context. We show that asymmetry in neuromast features and the rate of evolution is greater in cave-adapted species. Ancestral state reconstructions show that most Sinocyclocheilus are right-biased with some scatter, and show convergence of neuromast phenotypes. There is substantial variation in cephalic neuromast distribution patterns between and (to a lesser extent) within species. Behavioural assays show blind species have a distinctive wall-following behaviour. We explain these patterns in the context of the deep evolutionary history associated with this karstic region, other traits, and habitat occupation of these remarkable diversifications of fishes. Interestingly, some of these neuromast patterns and behaviour show convergence with other phylogenetically distant cavefish systems.

Comparative Mitogenomics of Fungal Species in Stachybotryaceae Provides Evolutionary Insights into Hypocreales

Stachybotrys chartarum is one of the world’s ten most feared fungi within the family Stachybotryaceae, although to date, not a single mitogenome has been documented for Stachybotryaceae. Herein, six mitogenomes of four different species in Stachybotryaceae are newly reported. The S. chartarum mitogenome was 30.7 kb in length and contained two introns (one each in rnl and cox1). A comparison of the mitogenomes of three different individuals of S. chartarum showed few nucleotide variations and conservation of gene content/order and intron insertion. A comparison of the mitogenomes of four different Stachybotryaceae species (Memnoniella echinata, Myrothecium inundatum, S. chartarum, and S. chlorohalonata), however, revealed variations in intron insertion, gene order/content, and nad2/nad3 joining pattern. Further investigations on all Hypocreales species with available mitogenomes showed greater variabilities in gene order (six patterns) and nad2/nad3 joining pattern (five patterns) although a dominant pattern always existed in each case. Ancestral state estimation showed that in each case the dominant pattern was always more ancestral than those rare patterns. Phylogenetic analyses based on mitochondrion-encoded genes supported the placement of Stachybotryaceae in Hypocreales. The crown age of Stachybotryaceae was estimated to be approximately the Early Cretaceous (141–142 Mya). This study greatly promotes our understanding of the evolution of fungal species in Hypocreales.