Lateral line placodes of aquatic vertebrates are evolutionarily conserved in mammals

Abstract

Placodes are focal thickenings of the surface ectoderm which, together with neural crest, generate the peripheral nervous system of the vertebrate head. Here we examine how, in embryonic mice, apoptosis contributes to the remodelling of the primordial posterior placodal area (PPA) into physically separated otic and epibranchial placodes. Using pharmacological inhibition of apoptosis-associated caspases, we find evidence that apoptosis eliminates hitherto undiscovered rudiments of the lateral line sensory system which, in fish and aquatic amphibia, serves to detect movements, pressure changes or electric fields in the surrounding water. Our results refute the evolutionary theory, valid for more than a century that the whole lateral line was completely lost in amniotes. Instead, those parts of the PPA which, under experimental conditions, escape apoptosis have retained the developmental potential to produce lateral line placodes and the primordia of neuromasts that represent the major functional units of the mechanosensory lateral line system.

Chicken embryos share mammalian patterns of apoptosis in the posterior placodal area

“…Thin dashed black lines, otic vesicle; b1/b2, branchial arches 1 and 2 that overgrow e1 and e2, respectively. Our findings strongly suggest, but do not yet conclusively prove, the hypothesis that apoptosis in the PPA of chicken embryos, as in mammals (Washausen & Knabe, 2018), eliminates vestigial lateral line placodes. This hypothesis is not inconsistent with our observation that differences of detail exist between the patterns of PPA apoptosis in chicken, mouse and T. belangeri.…”

“…; Washausen & Knabe, , , ). However, the nature of its functional contribution has been elusive for many years, and only recently has experimental evidence been provided that, in the PPA of mice, ‘phylogenetic cell death’ (Glücksmann, ) eliminates vestigial lateral line placodes with an astonishingly high developmental potential (Washausen & Knabe, ). The present work demonstrates that spatiotemporally regulated apoptosis also occurs in the PPA of chicken embryos.…”

“…In mammals, spatiotemporally regulated apoptosis accompanies placode morphogenesis in the PPA as well as in the anterior subsection of the panplacodal primordium (Washausen et al 2005;Knabe et al 2009;Washausen & Knabe, 2013, 2017, 2018. However, the nature of its functional contribution has been elusive for many years, and only recently has experimental evidence been provided that, in the PPA of mice, 'phylogenetic cell death' (Gl€ ucksmann, 1951) eliminates vestigial lateral line placodes with an astonishingly high developmental potential (Washausen & Knabe, 2018). The present work demonstrates that spatiotemporally regulated apoptosis also occurs in the PPA of chicken embryos.…”

“…Later, apoptosis is centred on the mature and regressing epibranchial placodes (Washausen et al. ; Washausen & Knabe, , , ). In T. belangeri , similar patterns of apoptosis accompany the morphogenesis of the trigeminal and lens placodes (Knabe et al.…”

“…To better understand why this is the case, we have examined how pharmacological inhibition of apoptosis‐associated caspases affects morphogenesis of the posterior placodes. Surprisingly, it turned out that ‘those parts of the PPA which, under experimental conditions, escape apoptosis have retained the developmental potential to produce lateral line placodes and the primordia of neuromasts’ (Washausen & Knabe, , p. 1). Hence, the evolutionary theory that the lateral line system which, in fish and aquatic amphibia, is responsible for the detection of movements, pressure changes or electric fields in the surrounding water (Northcutt, ; Schlosser, , ; Ghysen & Dambly‐Chaudière, ) was completely lost in amniotes (mammals, birds, reptiles) is no longer defensible (Washausen & Knabe, ).…”