Abstract
Manta rays and their relatives of the family Myliobatidae have pectoral fins that have been modified for underwater flight, as well as a pair of fleshy projections at the anterior of the body called cephalic lobes, which are specialized for feeding. As a unique trait with a dedicated function, cephalic lobes offer an excellent opportunity to elucidate the processes by which diverse body plans and features evolve. To shed light on the morphological development and genetic underpinnings of cephalic lobes, we examined paired fin development in cownose rays, which represent the sister taxon to manta rays in the genus Mobula. We find that cephalic lobes develop as anterior pectoral fin domains and lack independent posterior patterning by 5’ HoxD genes and Shh, indicating that cephalic lobes are not independent appendages but rather are modified pectoral fins. In addition, by leveraging interspecies comparative transcriptomics and domain-specific RNA-sequencing, we identify shared expression of anterior patterning genes, including Alx1, Alx4, Pax9, Hoxa13, Hoxa2 and Hoxd4, in the pectoral fins of cownose ray (Rhinoptera bonasus) and little skate (Leucoraja erinacea), providing evidence in support of a homologous relationship between the cephalic lobes of myliobatids and the anterior pectoral fins of skates. We also suggest candidate genes that may be involved in development of myliobatid-specific features, including Omd, which is likely associated with development of thick anterior pectoral fin radials of myliobatids, and Dkk1, which may inhibit tissue outgrowth at the posterior boundary of the developing cephalic lobes. Finally, we observe that cephalic lobes share a surprising number of developmental similarities with another paired fin modification: the claspers of male cartilaginous fishes, including enrichment of Hand2, Hoxa13, and androgen receptor. These results suggest that cephalic lobes may have evolved by co-opting developmental pathways that specify novel domains in paired fins. Taken together, these data on morphological development and comparative gene expression patterns illustrate how distinct body plans and seemingly novel features can arise via subtle changes to existing developmental pathways.
Highlights
IntroductionManta rays ( known as devil rays) and their relatives of the family Myliobatidae exhibit modified body plan features that arose in association with the evolution of oscillatory swimming and invasion of the pelagic environment (Rosenberger, 2001; Schaefer and Summers, 2005; Mulvany and Motta, 2013; Hall et al, 2018)
The stages of cownose ray fin development documented here are roughly analogous to stages 28–31 in bamboo sharks and catsharks (Ballard et al, 1993; Onimaru et al, 2018), though we note that sharks lack the anterior expansion of the pectoral fins characteristic of the Batoidea
We provide evidence supporting homology of myliobatid cephalic lobes with the anterior pectoral fins of rajid skates and suggest candidate genes that may be associated with development of the notch and the compagibus laminam, two features that are unique to the anterior pectoral fins of myliobatids
Summary
Manta rays ( known as devil rays) and their relatives of the family Myliobatidae exhibit modified body plan features that arose in association with the evolution of oscillatory swimming and invasion of the pelagic environment (Rosenberger, 2001; Schaefer and Summers, 2005; Mulvany and Motta, 2013; Hall et al, 2018). Myliobatid pectoral fins are laterally expanded, resulting in a high aspect ratio that reduces drag while increasing lift and thrust generation (Fontanella et al, 2013; Franklin et al, 2014), the center of mass is shifted anteriorly, which stabilizes the body during steady swimming (Fontanella et al, 2013), and the pectoral fins are stiffened by calcification patterns in the radials that redistribute load-bearing elements and increase the power of high amplitude pectoral strokes (Schaefer and Summers, 2005) Together, these modifications are associated with the evolution of oscillatory swimming, or underwater flight, the primary mode of locomotion in myliobatids
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