bioRxiv Science⌕ Search

Biology subjects

Todd, E. V.

Publications and source records attributed to Todd, E. V..

6 recordsLinked to original sources

Gonadal remodelling in socially driven sex change is associated with novel and known sex genes, epigenetic reprogramming, and inflammation-mediated apoptosis.

Many fish undergo dramatic, socially cued female-to-male sex change, yet the events that initiate and then regulate gonadal reprogramming and reorganisation during this phenomenal metamorphosis are broadly unknown. The New Zealand spotted wrasse, Notolabrus celidotus, is a temperate fish species that displays the extraordinary ability to undergo protogynous sex change. Removal of a terminal-phase male from a social group triggers the most dominant female to change sex and become a male. To characterise the molecular changes associated with gonadal metamorphosis in spotty, we used genomic and transcriptomic approaches, generating a high-quality genome and a transcriptomic time-series that captures the sex change process from start to finish. These data, together with paired histological data, reveal distinct transcriptional profiles that characterise the process of sex change. As expected, the expression of masculinising genes steadily increases, while feminising genes steadily decrease, throughout the transition. We further identify novel candidate genes, including genes involved in immune signalling and tissue remodelling through inflammation-mediated apoptosis, whose expression strongly correlates with key events in sex change, while also confirming the roles of known sex determination and differentiation genes in this process. Collectively these data give us new insights into how a normally committed developmental process remains plastic and is reversed to completely alter organ structures, and also sheds light on the evolution of sex determination in other animals. This work furthers the development of the spotty as a new tractable model for sex change research.

genomics↗

Behavioral and neural correlates of social hierarchy formation in a sex-changing fish

Social hierarchies in sex-changing fish determine which fish will change sex, yet the complexities of hierarchy formation at the neurobehavioral level are still being unraveled. Here, we investigate the formation of social hierarchies within groups of New Zealand spotty wrasse, integrating behavioral observations with neural activation patterns upon social disruption. We find that dominance hierarchies form linearly based on size, with larger fish displaying more dominant behaviors and smaller fish displaying more submissive behaviors. Disruption of the social hierarchy induced rapid behavioral changes, particularly in second-ranked fish, highlighting that second-ranked fish will opportunistically adopt a dominant position. Analysis of neural activation patterns reveals that the social decision-making network is deeply involved in the establishment of dominance, with the fish attaining dominance showing significant differences to all other ranked fish. Overall, this study underscores the complexity of social relationships and their neural underpinnings in the spotty wrasse, providing a foundation for further research into the cellular and molecular mechanisms of socially-controlled sex change, and demonstrates that disruption of the social hierarchy triggers rapid changes in both behavior and the social decision-making regions of the brain.

animal behavior and cognition↗

Differential sensory and immune gene evolution in sea turtles with contrasting demographic and life histories

Sea turtles represent an ancient lineage of marine vertebrates that evolved from terrestrial ancestors over 100 MYA, yet the genomic basis of the unique physiological and ecological traits enabling these species to thrive in diverse marine habitats remains largely unknown. Additionally, many populations have drastically declined due to anthropogenic activities over the past two centuries, and their recovery is a high global conservation priority. We generated and analyzed high-quality reference genomes for the leatherback (Dermochelys coriacea) and green (Chelonia mydas) turtles, representing the two extant sea turtle families. These genomes are highly syntenic and homologous, but localized regions of non-collinearity were associated with higher copy numbers of immune, zinc-finger, and olfactory receptor (OR) genes in green turtles, with ORs related to waterborne odorants greatly expanded in green turtles. Our findings suggest that divergent evolution of these key gene families may underlie immunological and sensory adaptations assisting navigation, occupancy of neritic versus pelagic environments, and diet specialization. Reduced collinearity was especially prevalent in microchromosomes, with greater gene content, heterozygosity, and genetic distances between species, supporting their critical role in vertebrate evolutionary adaptation. Finally, diversity and demographic histories starkly contrasted between species, indicating that leatherback turtles have had a low yet stable effective population size, exhibit extremely low diversity compared to other reptiles, and harbor a higher genetic load compared to green turtles, reinforcing concern over their persistence under future climate scenarios. These genomes provide invaluable resources for advancing our understanding of evolution and conservation best practices in an imperiled vertebrate lineage. Statement of significanceSea turtle populations have undergone recent global declines. We analyzed de novo assembled genomes for both extant sea turtle families through the Vertebrate Genomes Project to inform their conservation and evolutionary biology. These highly conserved genomes were differentiated by localized gene-rich regions of divergence, particularly within microchromosomes, suggesting that these genomic elements play key functional roles in the evolution of sea turtles and possibly other vertebrates. We further demonstrate that dissimilar evolutionary histories impact standing genomic diversity and genetic load, and are critical to consider when using these metrics to assess adaptive potential and extinction risk. Our results also demonstrate how reference genome quality impacts inferences of comparative and conservation genomics analyses that need to be considered in their application.

genomics↗

Sex change in the New Zealand spotty wrasse (Notolabrus celidotus), a temperate model species

The stunning sexual transformation commonly triggered by age, size or social context in some fishes is one of the best examples of phenotypic plasticity thus far described. To date our understanding of this process is dominated by studies on a handful of subtropical and tropical teleosts, often in wild settings because sex change has been challenging to achieve in captivity. Here we have established the protogynous New Zealand spotty wrasse, Notolabrus celidotus, as a temperate model for the experimental investigation of sex change. Captive fish were induced to change sex using either aromatase inhibition or manipulation of social groups. Complete transition from female to male occurred over 60 days and time-series sampling was used to quantify changes in hormone production, gene expression and gonadal cellular anatomy using radioimmunoassay, nanoString nCounter mRNA and histological analyses, respectively. Early-stage decreases in plasma 17{beta}-estradiol (E2) concentrations or gonadal aromatase (cyp19a1a) expression were not detected in spotty wrasse, despite these being commonly associated with the onset of sex change in subtropical and tropical protogynous (female-to-male) hermaphrodites. In contrast, expression of the masculinising factor amh (anti-Mullerian hormone) increased during early sex change, implying a potential role as a proximate trigger for masculinisation. Expression of male-related genes responsible for androgen production cyp11c1 and hsd11b2 increased from mid sex change. Gonadal expression of the glucocorticoid and mineralocorticoid receptors nr3c1 and nr3c2, putative mediators of the stress hormone cortisol, increased in late stages of sex change. Collectively, these data provide a foundation for the spotty wrasse as a temperate teleost model to study sex change and cell fate in vertebrates. Summary statementThe spotty wrasse, Notolabrus celidotus, is a new temperate model for the study of vertebrate sex change, this work characterises endocrine and genetic markers based on laboratory induced sex change.

physiology↗

An in vitro ovarian explant culture system to examine sex change in a hermaphroditic fish

Many teleost fishes undergo natural sex change, and elucidating the physiological and molecular controls of this process offers unique opportunities not only to develop methods of controlling sex in aquaculture settings, but to better understand vertebrate sexual development more broadly. Induction of sex change in some sequentially hermaphroditic or gonochoristic fish can be achieved in vivo through social manipulation, inhibition of aromatase activity, and steroid treatment. However, the induction of sex change in vitro has been largely unexplored. In this study, we established an in vitro culture system for ovarian explants in serum-free medium for a model sequential hermaphrodite, the New Zealand spotty wrasse (Notolabrus celidotus). This culture technique enabled evaluating the effect of various treatments with 17β-estradiol (E2), 11-ketotestosterone (11KT) or cortisol (CORT) on spotty wrasse ovarian architecture for 21 days. A quantitative approach to measuring the degree of ovarian atresia within histological images was also developed, using pixel-based machine learning software. Ovarian atresia likely due to culture was observed across all treatments including no-hormone controls, but was minimised with treatment of at least 10 ng/mL E2. Neither 11KT nor CORT administration induced proliferation of spermatogonia (i.e. sex change) in the cultured ovaries indicating culture beyond 21 days may be needed to induce sex change in vitro. The in vitro gonadal culture and analysis systems established here enable future studies investigating the paracrine role of sex steroids, glucocorticoids and a variety of other factors during gonadal sex change in fish.Abbreviations11KT11-ketestosterone;Ccontrol (no steroid);D0day 0 reference tissues;CORTcortisol;E217β-estradiol;HDF5hierarchical data format 5;IPinitial phase;PVOprevitellogenic oocytes;TPterminal phase.View Full Text

zoology↗

Stress, novel sex genes and epigenetic reprogramming orchestrate socially-controlled sex change

Bluehead wrasses undergo dramatic, socially-cued female to male sex change. We apply transcriptomic and methylome approaches in this wild coral reef fish to identify the primary trigger and subsequent molecular cascade of gonadal metamorphosis. Our data suggest that the environmental stimulus is exerted via the stress axis, that repression of the aromatase gene (encoding the enzyme converting androgens to estrogens) triggers a cascaded collapse of feminizing gene expression, and identifies notable sex-specific gene neofunctionalization. Furthermore, sex change involves distinct epigenetic reprogramming and an intermediate state with altered epigenetic machinery expression akin to the early developmental cells of mammals. These findings reveal at a molecular level how a normally committed developmental process remains plastic and is reversed to completely alter organ structures.\n\nOne Sentence SummaryOvary to testis transformation in a sex-changing fish involves transcriptomic and epigenomic reprogramming.

molecular biology↗