Gene expression differentiation in the reproductive tissues of Drosophila willistoni subspecies and their hybrids.

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. In Drosophila hybrids, how regulatory evolution impacts different reproductive tissues remains understudied. Here, we generate a new genome assembly and annotation in Drosophila willistoni and analyse the patterns of transcriptome divergence between two allopatrically evolved D. willistoni subspecies, 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 the D. willistoni X chromosome. Compared to the autosomes, the X chromosome 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 diverged D. willistoni subspecies and their hybrids provides a more nuanced view of early regulatory changes during speciation.

Hybrid male sterility between Drosophila willistoni species is caused by male failure to transfer sperm during copulation.

BACKGROUND: The biological concept of species stresses the importance of understanding what mechanisms maintain species reproductively isolated from each other. Often such mechanisms are divided into premating and postmating, with the latest being the result of either prezygotic or postzygotic isolation barriers. Drosophila willistoni quechua and Drosophila willistoni willistoni are two subspecies that experience reproductive isolation. When a D. w. quechua female is crossed with a D. w. willistoni male, the hybrid males (F1QW) are unable to father progeny; however, the reciprocal cross produces fertile hybrids. Thus, the mechanism of isolation is unidirectional hybrid male sterility. However, the sterile F1QW males contain large amounts of motile sperm. Here we explore whether pre-copulatory or post-copulatory pre-zygotic mechanisms serve as major deterrents in the ability of F1QW males to father progeny. RESULTS: Comparisons of parental and hybrid males copulation durations showed no significant reduction in copulation duration of F1QW males. Interrupted copulations of the parental species confirmed that sperm transfer occurs before the minimum copulation duration registered for F1QW males. However, we found that when females mate with F1QW males, sperm is not present inside the female storage organs and that the lack of sperm in storage is due to failure to transfer sperm rather than spillage or active sperm dumping by females. CONCLUSIONS: Sterility of F1QW hybrid males is primarily driven by their inability to transfer sperm during copulation.

The imprinted Igf2-Igf2r axis is critical for matching placental microvasculature expansion to fetal growth.

In all eutherian mammals, growth of the fetus is dependent upon a functional placenta, but whether and how the latter adapts to putative fetal signals is currently unknown. Here, we demonstrate, through fetal, endothelial, hematopoietic, and trophoblast-specific genetic manipulations in the mouse, that endothelial and fetus-derived IGF2 is required for the continuous expansion of the feto-placental microvasculature in late pregnancy. The angiocrine effects of IGF2 on placental microvasculature expansion are mediated, in part, through IGF2R and angiopoietin-Tie2/TEK signaling. Additionally, IGF2 exerts IGF2R-ERK1/2-dependent pro-proliferative and angiogenic effects on primary feto-placental endothelial cells ex vivo. Endothelial and fetus-derived IGF2 also plays an important role in trophoblast morphogenesis, acting through Gcm1 and Synb. Thus, our study reveals a direct role for the imprinted Igf2-Igf2r axis on matching placental development to fetal growth and establishes the principle that hormone-like signals from the fetus play important roles in controlling placental microvasculature and trophoblast morphogenesis.