Sex-biased gene expression and recent sex chromosome turnover

Cichlids are well known for their propensity to radiate generating arrays of morphologically and ecologically diverse species in short evolutionary time. Following this rapid evolutionary pace, cichlids show high rates of sex chromosome turnover. We here studied the evolution of sex-biased gene (SBG) expression in 14 recently diverged taxa of the Lake Tanganyika Tropheini cichlids, which show different XY sex chromosomes. Across species, sex chromosome sequence divergence predates divergence in expression between the sexes. Only one sex chromosome, the oldest, showed signs of demasculinization in gene expression and potentially contribution to the resolution of sexual conflict. SBGs in general showed high rates of turnovers and evolved mostly under drift. Sexual selection did not shape the rapid evolutionary changes of SBGs. Male-biased genes evolved faster than female-biased genes, which seem to be under more phylogenetic constraint. We found a relationship between the degree of sex bias and sequence evolution driven by sequence differences among the sexes. Consistent with other species, strong sex bias towards sex-limited expression contributes to resolving sexual conflict in cichlids. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)’.

Biogeographical patterns and speciation of the genus Pinguicula (Lentibulariaceae) inferred by phylogenetic analyses

Earlier phylogenetic studies in the genus Pinguicua (Lentibulariaceae) suggested that the species within a geographical region was rather monophyletic, although the sampling was limited or was restricted to specific regions. Those results conflicted with the floral morphology-based classification, which has been widely accepted to date. In the current study, one nuclear ribosomal DNA (internal transcribed spacer; ITS) and two regions of chloroplast DNA (matK and rpl32-trnL), from up to ca. 80% of the taxa in the genus Pinguicula, covering all three subgenera, were sequenced to demonstrate the inconsistency and explore a possible evolutionary history of the genus. Some incongruence was observed between nuclear and chloroplast topologies and the results from each of the three DNA analyses conflicted with the morphology-based subgeneric divisions. Both the ITS tree and network, however, corresponded with the biogeographical patterns of the genus supported by life-forms (winter rosette or hibernaculum formation) and basic chromosome numbers (haploidy). The dormant strategy evolved in a specific geographical region is a phylogenetic constraint and a synapomorphic characteristic within a lineage. Therefore, the results denied the idea that the Mexican group, morphologically divided into the three subgenera, independently acquired winter rosette formations. Topological incongruence among the trees or reticulations, indicated by parallel edges in phylogenetic networks, implied that some taxa originated by introgressive hybridisation. Although there are exceptions, species within the same geographical region arose from a common ancestor. Therefore, the classification by the floral characteristics is rather unreliable. The results obtained from this study suggest that evolution within the genus Pinguicula has involved; 1) ancient expansions to geographical regions with gene flow and subsequent vicariance with genetic drift, 2) acquirement of a common dormant strategy within a specific lineage to adapt a local climate (i.e., synapomorphic characteristic), 3) recent speciation in a short time span linked to introgressive hybridisation or multiplying the ploidy level (i.e., divergence), and 4) parallel evolution in floral traits among lineages found in different geographical regions (i.e., convergence). As such, the floral morphology masks and obscures the phylogenetic relationships among species in the genus.

Rubisco adaptation is more limited by phylogenetic constraint than by catalytic trade-off

Rubisco assimilates CO2 to form the sugars that fuel life on earth. Correlations between rubisco kinetic traits across species have led to the proposition that rubisco adaptation is highly constrained by catalytic trade-offs. However, these analyses did not consider the phylogenetic context of the enzymes that were analysed. Thus, it is possible that the correlations observed were an artefact of the presence of phylogenetic signal in rubisco kinetics and the phylogenetic relationship between the species that were sampled. Here, we conducted a phylogenetically-resolved analysis of rubisco kinetics and show that there is a significant phylogenetic signal in rubisco kinetic traits. We re-evaluated the extent of catalytic trade-offs accounting for this phylogenetic signal and found that all were attenuated. Following phylogenetic correction, the largest catalytic trade-offs were observed between the Michaelis constant for CO2 and carboxylase turnover (∼21-37%), and between the Michaelis constants for CO2 and O2 (∼9-19%), respectively. All other catalytic trade-offs were substantially attenuated such that they were marginal (<9%) or non-significant. This phylogenetically resolved analysis of rubisco kinetic evolution also identified kinetic changes that occur concomitant with the evolution of C4 photosynthesis. Finally, we show that phylogenetic constraints have played a larger role than catalytic trade-offs in limiting the evolution of rubisco kinetics. Thus, although there is strong evidence for some catalytic trade-offs, rubisco adaptation has been more limited by phylogenetic constraint than by the combined action of all such trade-offs.

Extreme Morphology, Functional Trade-Offs, and Evolutionary Dynamics in a Clade of Open-Ocean Fishes (Perciformes: Bramidae)

When novel or extreme morphologies arise, they are oft met with the burden of functional trade-offs in other aspects of anatomy, which may limit phenotypic diversification and make particular adaptive peaks inaccessible. Bramids (Perciformes: Bramidae) comprise a small family of 20 extant species of fishes, which are distributed throughout pelagic waters worldwide. Within the Bramidae, the fanfishes (Pteraclis and Pterycombus) differ morphologically from the generally stout, laterally compressed species that typify the family. Instead, Pteraclis and Pterycombus exhibit extreme anterior positioning of the dorsal fin onto the craniofacial skeleton. Consequently, they possess fin and skull anatomies that are radically different from other bramid species. Here, we investigate the anatomy, development, and evolution of the Bramidae to test the hypothesis that morphological innovations come at functional (proximate) and evolutionary (ultimate) costs. Addressing proximate effects, we find that the development of an exaggerated dorsal fin is associated with neurocrania modified to accommodate an anterior expansion of the dorsal fin. This occurs via reduced development of the supraoccipital crest (SOC), providing a broad surface area on the skull for insertion of the dorsal fin musculature. While these anatomical shifts are presumably associated with enhanced maneuverability in fanfishes, they are also predicted to result in compromised suction feeding, possibly limiting the mechanisms of feeding in this group. Phylogenetic analyses suggest craniofacial and fin morphologies of fanfishes evolved rapidly and are evolutionarily correlated across bramids. Furthermore, fanfishes exhibit a similar rate of lineage diversification as the rest of the Bramidae, lending little support for the prediction that exaggerated medial fins are associated with phylogenetic constraint. Our phylogeny places fanfishes at the base of the Bramidae and suggests that non-fanfish bramids have reduced medial fins and re-evolved SOCs. These observations suggest that the evolution of novel fin morphologies in basal species has led to the phylogenetic coupling of head and fin shape, possibly predisposing the entire family to a limited range of feeding. Thus, the evolution of extreme morphologies may have carry-over effects, even after the morphology is lost, limiting ecological diversification of lineages.

Phylogenetic comparison of egg transparency in ascidians by hyperspectral imaging

The transparency of animals is an important biological feature. Ascidian eggs have various degrees of transparency, but this characteristic has not yet been measured quantitatively and comprehensively. In this study, we established a method for evaluating the transparency of eggs to first characterize the transparency of ascidian eggs across different species and to infer a phylogenetic relationship among multiple taxa in the class Ascidiacea. We measured the transmittance of 199 eggs from 21 individuals using a hyperspectral camera. The spectrum of the visual range of wavelengths (400–760 nm) varied among individuals and we calculated each average transmittance of the visual range as bio-transparency. When combined with phylogenetic analysis based on the nuclear 18S rRNA and the mitochondrial cytochrome c oxidase subunit I gene sequences, the bio-transparencies of 13 species were derived from four different families: Ascidiidae, Cionidae, Pyuridae, and Styelidae. The bio-transparency varied 10–90% and likely evolved independently in each family. Ascidiella aspersa showed extremely high (88.0 ± 1.6%) bio-transparency in eggs that was maintained in the “invisible” larva. In addition, it was indicated that species of the Ascidiidae family may have a phylogenetic constraint of egg transparency.

RuBisCO adaptation is more limited by phylogenetic constraint than by catalytic trade-off in plants

RuBisCO assimilates CO2 to form the sugars that fuel life on earth. Correlations between RuBisCO kinetic traits across species have led to the proposition that RuBisCO adaptation is constrained by catalytic trade-offs. However, these analyses did not consider the phylogenetic context of the enzymes that were analysed. Thus, it is possible that the observed correlations between RuBisCO kinetic traits are an artefact of the presence of phylogenetic signal in RuBisCO kinetics and the phylogenetic relationship between the species that were sampled. Here, we conducted a phylogenetically resolved analysis of RuBisCO kinetics and show that there is significant phylogenetic signal in all carboxylase kinetic traits, and significant phylogenetic signal in the Michaelis constant for O2 in species that conduct C3 photosynthesis. When accounting for this phylogenetic non-independence between enzymes, we show that the catalytic trade-off between carboxylase turnover and the Michaelis constant for CO2 is weak (~30 % dependency) and that the correlations between all other RuBisCO kinetic traits are either not-significant or marginal (<9 % dependency). Finally, we demonstrate that phylogenetic constraints have limited RuBisCO evolution to a greater extent than catalytic trade-offs. Thus, RuBisCO adaptation in angiosperms is predominantly limited by phylogenetic constraint (most likely caused by a slow rate of molecular evolution) and a partial trade-off between carboxylase turnover and the Michaelis constant for CO2.

Wood anatomy of the neotropical liana lineage Paullinia L. (Sapindaceae)

The liana genus Paullinia L. is one of the most speciose in the neotropics and is unusual in its diversity of stem macromorphologies and cambial conformations. These so-called “vascular cambial variants” are morphologically disparate, evolutionarily labile, and are implicated in injury repair and flexibility. In this study, we explore at the finer scale how wood anatomy translates into functions related to the climbing habit. We present the wood anatomy of Paullinia and discuss the functional implications of key anatomical features. Wood anatomy characters were surveyed for 21 Paullinia species through detailed anatomical study. Paullinia woods have dimorphic vessels, rays of two size classes, and both septate and non-septate fibers. Fibriform vessels, fusiform axial parenchyma, and elements morphologically intermediate between fibers and axial parenchyma were observed. Prismatic crystals are common in the axial and/or ray parenchyma, and laticifers are present in the cortex and/or the early-formed secondary phloem. Some features appear as unique to Paullinia or the Sapindaceae, such as the paucity of axial parenchyma and the abundance of starch storing fibers. Although many features are conserved across the genus, the Paullinia wood anatomy converges on several features of the liana-specific functional anatomy expressed across distantly related lianas, demonstrating an example of convergent evolution. Hence, the conservation of wood anatomy in Paullinia suggests a combination of phylogenetic constraint as a member of Sapindaceae and functional constraint from the liana habit.

Evolution and genetic basis of the plant-penetrating ovipositor, a key adaptation in the transition to herbivory within the Drosophilidae

Herbivorous insects are extraordinarily diverse, yet are found in only one-third of insect orders. This skew may be driven by barriers to plant colonization coupled with phylogenetic constraint on plant-colonizing adaptations. Physical barriers can be surmounted by key innovations like the plant-penetrating ovipositor. Within Drosophilidae, ovipositor margins densely adorned with hard bristles used to cut into plants evolved repeatedly, but their evolutionary, developmental and genomic basis has only been explored in Drosophila suzukii. Here, we addressed this gap using Scaptomyza, an herbivorous radiation nested in a detritivorous clade. First, we found that ovipositor bristle number increased markedly as herbivory evolved in Scaptomyza. We then dissected the genomic architecture of variation in ovipositor bristle number within S. flava using a pooled genome wide association study (pool-GWAS). Variation in ovipositor bristle number in S. flava was heritable and associated with single nucleotide polymorphisms (SNPs) within non-coding regions involved in neural development. Genotyping of individual flies replicated the association at a candidate SNP upstream of Gai, a neural development gene, and estimated that it contributes to an average gain of ∼0.58 bristles/ovipositor in S. flava. Neural developmental genes thus underlie variation in this key morphological adaptation, possibly facilitating the evolution of this trait and the colonization of tough tissue of living plants.