An official website of the United States government
Abstract Early lineage diversification is central to understand what mutational events drive species divergence. Particularly, gene misregulation in interspecific hybrids can inform about what genes and pathways underlie hybrid dysfunction. InDrosophilahybrids, how regulatory evolution impacts different reproductive tissues remains understudied. Here, we generate a new genome assembly and annotation inDrosophila willistoniand analyse the patterns of transcriptome divergence between two allopatrically evolvedD. willistonisubspecies, their male sterile and female fertile hybrid progeny across testis, male accessory gland, and ovary. Patterns of transcriptome divergence and modes of regulatory evolution were tissue‐specific. Despite no indication for cell‐type differences in hybrid testis, this tissue exhibited the largest magnitude of expression differentiation between subspecies and between parentals and hybrids. No evidence for anomalous dosage compensation in hybrid male tissues was detected nor was a differential role for the neo‐ and the ancestral arms of theD. willistoni Xchromosome. Compared to the autosomes, theXchromosome appeared enriched for transgressively expressed genes in testis despite being the least differentiated in expression between subspecies. Evidence for fine genome clustering of transgressively expressed genes suggests a role of chromatin structure on hybrid gene misregulation. Lastly, transgressively expressed genes in the testis of the sterile male progeny were enriched for GO terms not typically associated with sperm function, instead hinting at anomalous development of the reproductive tissue. Our thorough tissue‐level portrait of transcriptome differentiation between recently divergedD. willistonisubspecies and their hybrids provides a more nuanced view of early regulatory changes during speciation.
more »
« less
A developmental atlas of male terminalia across twelve species of Drosophila
How complex morphologies evolve is one of the central questions in evolutionary biology. Observing the morphogenetic events that occur during development provides a unique perspective on the origins and diversification of morphological novelty. One can trace the tissue of origin, emergence, and even regression of structures to resolve murky homology relationships between species. Here, we trace the developmental events that shape some of the most diverse organs in the animal kingdom—the male terminalia (genitalia and analia) ofDrosophilids. Male genitalia are known for their rapid evolution with closely related species of theDrosophilagenus demonstrating vast variation in their reproductive morphology. We used confocal microscopy to monitor terminalia development during metamorphosis in twelve related species ofDrosophila. From this comprehensive dataset, we propose a new staging scheme for pupal terminalia development based on shared developmental landmarks, which allows one to align developmental time points between species. We were able to trace the origin of different substructures, find new morphologies and suggest possible homology of certain substructures. Additionally, we demonstrate that posterior lobe is likely originated prior to the split between theDrosophila melanogasterand theDrosophila yakubaclade. Our dataset opens up many new directions of research and provides an entry point for future studies of theDrosophilamale terminalia evolution and development.
more »
« less
- Award ID(s):
- 2129903
- PAR ID:
- 10507762
- Publisher / Repository:
- Frontiers
- Date Published:
- Journal Name:
- Frontiers in Cell and Developmental Biology
- Volume:
- 12
- ISSN:
- 2296-634X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract BackgroundOne goal of evolutionary developmental biology is to understand the role of development in the origin of phenotypic novelty and convergent evolution. Geckos are an ideal system to study this topic, as they are species‐rich and exhibit a suite of diverse morphologies—many of which have independently evolved multiple times within geckos. ResultsWe characterized and discretized the embryonic development ofLepidodactylus lugubris—an all‐female, parthenogenetic gecko species. We also used soft‐tissue μCT to characterize the development of the brain and central nervous system, which is difficult to visualize using traditional microscopy techniques. Additionally, we sequenced and assembled a de novo transcriptome for a late‐stage embryo as a resource for generating future developmental tools. Herein, we describe the derived and conserved patterns ofL. lugubrisdevelopment in the context of squamate evolution and development. ConclusionsThis embryonic staging series, μCT data, and transcriptome together serve as critical enabling resources to study morphological evolution and development, the evolution and development of parthenogenesis, and other questions concerning vertebrate evolution and development in an emerging gecko model.more » « less
-
Abstract Genital evolution can be driven by diverse selective pressures. Across taxa we see evidence of covariation between males and females, as well as divergent genital morphologies between closely related species. Quantitative analyses of morphological changes in coevolving male and female genitalia have not yet been shown in vertebrates. This study uses 2D and 3D geometric morphometrics to quantitatively compare the complex shapes of vaginal pouches and hemipenes across three species of watersnakes (the sister taxa Nerodia fasciata, N. sipedon, and a close relative N. rhombifer) to address the relationship between genital morphology and divergence time in a system where sexual conflict may have driven sexually antagonistic coevolution of genital traits. Our pairwise comparisons of shape differences across species show that the sister species have male and female genitalia that are significantly different from each other, but more similar to each other than to N. rhombifer. We also determine that the main axes of shape variation are the same for males and females, with changes that relate to deeper bilobation of the vaginal pouch and hemipenes. In males, the protrusion of the region of spines at the base of the hemipene trades off with the degree of bilobation, suggesting amelioration of sexual conflict, perhaps driven by changes in the relative size of the entrance of the vaginal pouch that could have made spines less effective.more » « less
-
Summary Replicated trait evolution can provide insights into the mechanisms underlying the evolution of biodiversity. One example of replicated evolution is the awn, an organ elaboration in grass inflorescences.Awns are likely homologous to leaf blades. We hypothesized that awns have evolved repeatedly because a conserved leaf blade developmental program is continuously activated and suppressed over the course of evolution, leading to the repeated emergence and loss of awns. To evaluate predictions arising from our hypothesis, we used ancestral state estimations, comparative genetics, anatomy, and morphology to trace awn evolution.We discovered that awned lemmas that evolved independently share similarities in developmental trajectory. In addition, in two species with independently derived awns and differing awn morphologies (Brachypodium distachyonandAlopecurus myosuroides), we found that orthologs of theYABBYtranscription factor geneDROOPING LEAFare required for awn initiation. Our analyses of awn development inBrachypodium distachyon,Alopecurus myosuroides, andHolcus lanatusalso revealed that differences in the relative expansion of awned lemma compartments can explain diversity in awn morphology at maturity.Our results show that developmental conservation can underlie replicated evolution and can potentiate the evolution of morphological diversity.more » « less
-
Background: One goal of evolutionary developmental biology is to understand the role of development in the origin of phenotypic novelty and convergent evolution. Geckos are an ideal system to study this topic, as they are species-rich and exhibit a suite of diverse morphologies — many of which have independently evolved multiple times within geckos. Results: We characterized and discretized the embryonic development of Lepidodactylus lugubris - an all-female, parthenogenetic gecko species. We also used soft-tissue μCT to characterize the development of the brain and central nervous system, which is difficult to visualize using traditional microscopy techniques. Additionally, we sequenced and assembled a de novo transcriptome for a late-stage embryo as a resource for generating future developmental tools. Herein, we describe the derived and conserved patterns of L. lugubris development in the context of squamate evolution and development. Conclusions: This embryonic staging series, μCT data, and transcriptome together serve as critical enabling resources to study morphological evolution and development, the evolution and development of parthenogenesis, and other questions concerning vertebrate evolution and development in an emerging gecko model.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/fcell.2024.1349275
