Abstract
BackgroundHeterochronic shifts during ontogeny can result in adaptively important innovations and might be initiated by simple developmental switches. Understanding the nature of these developmental events can provide insights into fundamental molecular mechanisms of evolutionary change. Fishes from the Suborder Belonoidei display a vast array of extreme craniofacial morphologies that appear to have arisen through a series of heterochronic shifts. We performed a molecular heterochrony study, comparing postembryonic jaw development in representatives of the Suborder Belonoidei, the halfbeak Dermogenys pusilla (where the lower jaw is considerably elongated compared to the upper jaw) and the needlefish Belone belone (where both jaws are elongated), to a representative of their sister group the Suborder Adrianichthyoidei, the medaka Oryzias latipes, which has retained the ancestral morphology.ResultsEarly in development, the lower jaw displays accelerated growth both in needlefish and halfbeak compared to medaka, and secondary acceleration of the upper jaw is seen in needlefish later in their development, representing a case of mosaic heterochrony. We identified toothless extensions of the dentaries as innovations of Belonoid fishes and the source of heterochronic growth. The molecular basis of growth heterochronies in the Belonoidei was examined through comparing expression of skeletogenic genes during development of halfbeak and medaka. The calmodulin paralogue calm1 was identified as a potential regulator of jaw length in halfbeak as its expression gradually increases in the lower jaw, but not the upper jaw, in a pattern that matches its outgrowth. Moreover, medaka displays equal expression of calm1 in the upper and lower jaws, consistent with the lack of jaw outgrowth in this species.ConclusionsHeterochronic shifts in jaw growth have occurred repeatedly during the evolution of Belonoid fishes and we identify toothless extensions of the dentaries as an important innovation of this group. Our results suggest that calm1 contributes to jaw heterochrony in halfbeak, potentially driving further heterochronic shifts in jaw growth across the Suborder Belonoidei, such as the upper jaw acceleration observed in needlefish.
Highlights
Heterochronic shifts during ontogeny can result in adaptively important innovations and might be initiated by simple developmental switches
We developed a set of housekeeping genes (HKG), testing previous HKGs used for qRT-PCR on cichlid pharyngeal jaws [45], plus β-actin and gapdh
Characterizing growth heterochronies in halfbeak and needlefish The relationship between jaw shape and age was examined in D. pusilla, O. latipes and B. belone, through plotting ratios between lower and upper jaws against scaled age using a method modified from [23]
Summary
Heterochronic shifts during ontogeny can result in adaptively important innovations and might be initiated by simple developmental switches. By applying a comparative framework, molecular studies of heterochrony have the potential to identify the ontogenetic stage, structure and magnitude of growth of morphological alterations, and their genetic bases This approach involves developmental comparisons between members of different lineages to their sister lineages that retained the ancestral condition (for examples see [8,12,13,14,15]). Heterochronic growth may be underlain by various developmental mechanisms that alter the proliferation, differentiation or apoptosis of various cell populations and as such, identifying its genetic basis can be aided by a fine-scaled developmental approach [4,16] Such developmental investigations have been successfully utilized in studies in cichlid fish and Galapagos finches, which interestingly, point at similar molecular drivers of differential proliferation in cellular condensations that contribute to shape differences in adult jaws and beaks respectively (that is, bmp and calmodulin) [17,18,19,20,21,22]
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