Search bioRxiv⌕ Search

Biology subjects

Kingsley, E. P.

Publications and source records attributed to Kingsley, E. P..

3 recordsLinked to original sources

Integration of sexual dimorphism and left-right asymmetry in the development of the duck syrinx

Embryonic morphogenesis is regulated across multiple dimensions. In ducks, the syrinx, the avian vocal organ, undergoes morphogenic processes that result in both left-right asymmetric and sexually dimorphic development. Although these properties are thought to be controlled by the NODAL-PITX2 left-right signaling cascade and the sex steroid pathways, how these mechanisms work together to produce an asymmetric structure in a sexually dimorphic manner remains unclear. Here, we first establish evidence for sexual selection driving the evolution of the duck syrinx. During its development, we observe that PITX2 is expressed on the left side in both male and female ducks, although not in other birds. Asymmetric activation of PITX2 in this domain is triggered by bilateral BMP signaling but is limited to the left side by left-specific stably accessible chromatin established during an earlier asymmetric wave of PITX2 expression. Ultimately, there is an induction of left-specific WNT and BMP signaling in the syrinx primordium, which synergistically elevates cell proliferation on the left, leading to asymmetric growth. Estrogen receptor expression is also shown to be induced on the left side of the forming syrinx. This has no effect in males, but in females where the hormone is present, estrogen signaling reduces left-sided cell proliferation, thus promoting bilaterally symmetric growth. These data demonstrate how sexually dimorphic left-right asymmetry can be integrated to produce an adaptive trait.

developmental biology↗

A dynamic Hedgehog gradient orients tracheal cartilage rings

The patterning of periodic stripes during embryonic development generates similar structures that repeat at regular spatial intervals within a tissue. These patterns are often attributed to a Turing-like mechanism, which self-organizes characteristically spaced stripes, but these patterns are predicted to be disorganized. Conversely, well-oriented, parallel stripes are often observed in nature. We investigate this phenomenon during the formation of the cartilage rings that support the amniote airway. We find evidence that a Turing-like mechanism underpins the formation of the repeating cartilage elements. Additionally, SHH is transiently expressed in a thin dorsal domain along the length of the developing trachea, resulting in a dorsoventral gradient of Hedgehog activity that recedes over time. Using mathematical modelling, we predict that the spatiotemporal dynamics of the gradient are required to organize the stripes into parallel rings. Comparing in silico predictions with experimental SHH manipulations shows that the Hedgehog gradient is essential for proper tracheal cartilage patterning.

developmental biology↗

Adaptive tail-length evolution in deer mice is associated with differential Hoxd13 expression in early development

Variation in the size and number of axial segments underlies much of the diversity in animal body plans. Here, we investigate the evolutionary, genetic, and developmental mechanisms driving tail-length differences between forest and prairie ecotypes of deer mice (Peromyscus maniculatus). We first show that long-tailed forest mice perform better in an arboreal locomotion assay, consistent with tails being important for balance during climbing. The long tails of these forest mice consist of both longer and more caudal vertebrae than prairie mice. Using quantitative genetics, we identify six genomic regions that contribute to differences in total tail length, three of which associate with vertebra length and the other three with vertebra number. For all six loci, the forest allele increases tail length, consistent with the cumulative effect of natural selection. Two of the genomic regions associated with variation in vertebra number contain Hox gene clusters. Of those, we find an allele-specific decrease in Hoxd13 expression in the embryonic tail bud of long-tailed forest mice, consistent with its role in axial elongation. Additionally, we find that forest embryos have more presomitic mesoderm than prairie embryos, and that this correlates with an increase in the number of neuromesodermal progenitors (NMPs), which are modulated by Hox13 paralogs. Together, these results suggest a role for Hoxd13 in the development of natural variation in adaptive morphology on a microevolutionary timescale. HIGHLIGHTSO_LIIn deer mice, the long-tailed forest ecotype outperforms the short-tailed prairie ecotype in climbing, consistent with the tails role in balance. C_LIO_LILong tails are due to mutations on distinct chromosomes that affect either length or number of caudal vertebrae. C_LIO_LIQTL mapping identifies Hox clusters, one gene of which - Hoxd13 - shows low allele-specific expression in the embryonic tail bud of forest mice. C_LIO_LIForest mouse embryos have a larger presomitic mesoderm (PSM), likely mediated by a larger progenitor population (NMPs) and lower Hoxd13 levels. C_LI

genetics↗