Arrested development inXenopus laevistadpoles: how size constrains metamorphosis

Abstract

SUMMARY Xenopus laevis tadpoles that arrest development and remain as larvae for several years sometimes occur spontaneously in laboratory populations. These tadpoles cease development at an early hindlimb stage, but continue to grow and develop into grossly deformed giants. Giant tadpoles lack thyroid glands, and differ in morphology and behaviour from normal larvae. They are negatively buoyant, typically with small and partially solidified lungs, and have greatly enlarged fat bodies. Giant tadpoles have mature gonads with eggs and sperm, whereas normal tadpoles of the same stage have undifferentiated gonads. Larval reproduction has never been reported in anurans, but gonadal development decoupled from metamorphosis brings these giants the closest of any anurans to being truly neotenic. We discuss behavioural and morphological factors that may hinder both reproduction in giant Xenopus larvae and the evolution of neoteny in anurans in general. Experimental treatment with exogenous thyroid hormone induces some,but not complete, metamorphic changes in these giants. The limbs and head progress through metamorphosis; however, all tadpoles die at the stage when the tail would normally be resorbed. The disproportionate growth of tissues and organs in giant tadpoles may preclude complete metamorphosis, even under exogenous thyroid hormone induction.

The ontogeny of Pseudis platensis (Anura, Hylidae): Heterochrony and the effects of larval development on postmetamorphic life

“…In a study of exceptionally old (8 years old) giant tadpoles of Xenopus laevis that lacked thyroid glands, Rot-Nikcevic and Wassersug (2004) found mature gonads with eggs and sperm, whereas normal tadpoles of the same stage had undifferentiated gonads. In this case, prolonged period of larval development may have been a factor permitting gonad maturation.…”

“…Many authors, e.g., Reilly et al (1997), Ogielska and Kotusz (2004), and Rot-Nikcevic and Wassersug (2004), noted that gonad development may be decoupled from somatic development and/or metamorphosis. Paedomorphosis (as was described in the urodele Ambystoma; Reilly et al, 1997), represents a heterochronic event in which the disappearance of some somatic larval features is decelerated.…”

“…However, these giant tadpoles were unable to metamorphose and reproduce. The disproportionate growth of tissues and organs appeared to be the factor precluding successful metamorphosis (Rot-Nikcevic and Wassersug, 2004). Normal giant tadpoles, such as P. platensis, were described in the extinct pipoid Paleobatrachus (Roček et al, 2006).…”

p27BBP/eIF6 acts as an anti-apoptotic factor upstream of Bcl-2 during Xenopus laevis development

“…It should be noted, however, that specific counts in hepatocytes and fat cells could not be performed in adult Xenopus to parallel the eIF6 þ /À mice observations. 5 Indeed, in Xenopus embryos, liver cells differentiate at stage 46, 25 when the bent phenotype had recovered and fat cells appear following metamorphosis (see Rot-Nikcevic and Wassersug 26 ).…”

Reversible developmental stasis in response to nutrient availability in theXenopus laevisCNS

“…In amphibians, where development of the tadpole larva occurs externally, maternal nutrition in Xenopus is required for neuronal development and function up to stage 45 (Igarashi et al, 2015). For tadpoles, chronic low food conditions negatively affect growth and delay metamorphosis (Rot-Nikcevic and Wassersug, 2004;Warne and Crespi, 2015;Wright et al, 2011). Yet little is known about the effects of fluctuations in nutrient availability on early amphibian growth and development, or the specific consequences of nutrient restriction on the developing brain.…”