One hundred million years of skin feeding? Extended parental care in a Neotropical caecilian (Amphibia: Gymnophiona)

Abstract

Maternal dermatophagy, the eating of maternal skin by offspring, is an unusual form of parental investment involving co-evolved specializations of both maternal skin and offspring dentition, which has been recently discovered in an African caecilian amphibian. Here we report the discovery of this form of parental care in a second, distantly related Neotropical species Siphonops annulatus, where it is characterized by the same syndrome of maternal and offspring specializations. The detailed similarities of skin feeding in different caecilian species provide strong evidence of its homology, implying its presence in the last common ancestor of these species. Biogeographic considerations, the separation of Africa and South American land masses and inferred timescales of amphibian diversification all suggest that skin feeding is an ancient form of parental care in caecilians, which has probably persisted in multiple lineages for more than 100 Myr. These inferences support the hypotheses that (i) maternal dermatophagy is widespread in oviparous direct-developing caecilians, and (ii) that viviparous caecilians that feed on the hypertrophied maternal oviduct evolved from skin-feeding ancestors. In addition to skin-feeding, young S. annulatus were observed to congregate around, and imbibe liquid exuded from, the maternal cloacal opening.

Evolution of Cranial Shape in Caecilians (Amphibia: Gymnophiona)

“…Müller et al 2005;Müller 2006a;Müller et al 2009), life-history (e.g. Kupfer et al 2005;Kupfer et al 2006b;Wilkinson et al 2008;Kuehnel and Kupfer 2012;Gomes et al 2013), phylogeny (e.g. Gower et al 2002;San Mauro et al 2004;Roelants et al 2007;Loader et al 2011;Maddin et al 2012b) and ecology (e.g.…”

The evolution of parental investment in caecilian amphibians: a comparative approach

“…Post-hatching parental care of oviparous caecilians is also advantageous when the skull and body development of initially altricial hatchlings is being completed under maternal care (Kupfer et al, 2006;M€ uller, 2007;Wilkinson et al, 2008). Apparently, maternal dermatotrophy is associated with reduced investment in egg size; thus, the time of egg development is likely shortened as well compared to largeyolked (macrolecithal) eggs of indirectly and directly developing caecilians.…”

“…Other directly developing caecilians have altricial hatchlings, which are nursed via the maternal skin (i.e. maternal dermatotrophy) (Kupfer et al, 2006;Wilkinson et al, 2008) until they become independent. A considerable number of caecilians exhibit viviparity, with at least two distinguishable modes of viviparity characterized by differences in the independence of the newborn (Wake, 1980;Loader et al, 2003;M€ uller et al, 2009).…”

Morphology and Herpetology: How and Why They Interact

“…Juvenile teeth are modified to obtain nutrition from maternal skin and the skin is modified to provide nourishment. Wilkinson et al (2008) conjectured that skin-feeding may be an ancestral trait, lost in many lineages, preceding the evolution of oviductal viviparity. An equally parsimonious alternative hypothesis is that skin feeding has arisen independently several times (but does not presage viviparity) by utilizing common maternal skin responses to hormones coupled with birth at a relatively altricial state (analogous to the situation in back-brooding seen in pipid and amphignathodontid and allied frogs).…”

“…Perhaps the most dramatic new discovery in caecilian biology is that of newly hatched young in distantly related lineages that feed on the hypertrophied, lipidized skin of their mothers (Kupfer et al, 2006Wilkinson et al, 2008), meshing studies of feeding and teeth. Juvenile teeth are modified to obtain nutrition from maternal skin and the skin is modified to provide nourishment.…”