Distinct Patterns of Desynchronized Limb Regression in Malagasy Scincine Lizards (Squamata, Scincidae)

Abstract

Scincine lizards in Madagascar form an endemic clade of about 60 species exhibiting a variety of ecomorphological adaptations. Several subclades have adapted to burrowing and convergently regressed their limbs and eyes, resulting in a variety of partial and completely limbless morphologies among extant taxa. However, patterns of limb regression in these taxa have not been studied in detail. Here we fill this gap in knowledge by providing a phylogenetic analysis of DNA sequences of three mitochondrial and four nuclear gene fragments in an extended sampling of Malagasy skinks, and microtomographic analyses of osteology of various burrowing taxa adapted to sand substrate. Based on our data we propose to (i) consider Sirenoscincus Sakata & Hikida, 2003, as junior synonym of Voeltzkowia Boettger, 1893; (ii) resurrect the genus name Grandidierina Mocquard, 1894, for four species previously included in Voeltzkowia; and (iii) consider Androngo Brygoo, 1982, as junior synonym of Pygomeles Grandidier, 1867. By supporting the clade consisting of the limbless Voeltzkowia mira and the forelimb-only taxa V. mobydick and V. yamagishii, our data indicate that full regression of limbs and eyes occurred in parallel twice in the genus Voeltzkowia (as hitherto defined) that we consider as a sand-swimming ecomorph: in the Voeltzkowia clade sensu stricto the regression first affected the hindlimbs and subsequently the forelimbs, whereas the Grandidierina clade first regressed the forelimbs and subsequently the hindlimbs following the pattern prevalent in squamates. Timetree reconstructions for the Malagasy Scincidae contain a substantial amount of uncertainty due to the absence of suitable primary fossil calibrations. However, our preliminary reconstructions suggest rapid limb regression in Malagasy scincids with an estimated maximal duration of 6 MYr for a complete regression in Paracontias, and 4 and 8 MYr respectively for complete regression of forelimbs in Grandidierina and hindlimbs in Voeltzkowia.

Descriptive osteology and patterns of limb loss of the European limbless skink Ophiomorus punctatissimus (Squamata, Scincidae)

“…Remarkably, a very similar condition of the pelvis is present in the Malagasy mermaid skink Voeltzkowia mobydick (Miralles et al. , ), which is devoid of hindlimbs similarly to O . punctatissimus .…”

“…; Siler & Brown, ; Miralles et al. , ). Within Scincidae, the genus Ophiomorus exhibits a highly interspecifically variable degree of limb reduction, but the reduction of digits, if present, is stronger in the hindlimbs than in the forelimbs (Greer & Wilson, ).…”

“…Limb loss and reduction evolved at least 16-20 times independently across Scincidae, corresponding to a very high frequency of convergent limb loss among squamates (Wiens et al 2006;Siler & Brown, 2011;Miralles et al 2012Miralles et al , 2015. Within Scincidae, the genus Ophiomorus exhibits a highly interspecifically variable degree of limb reduction, but the reduction of digits, if present, is stronger in the hindlimbs than in the forelimbs (Greer & Wilson, 2001).…”

Species delimitation methods put into taxonomic practice: two new Madascincus species formerly allocated to historical species names (Squamata, Scincidae)

“…5). It should nevertheless be highlighted that due to the presence of one outlier sample in the Miralles and Vences (2015) data set, which unambiguously clustered with the northern clade but geographically is nested within the central clade distribution area (in An'Ala, a locality relatively close to the type locality of M. melanopleura), we cannot totally discard the possible -past or present -sympatric occurrence of M. minutus at Anzahamaru.…”

“…These lizards likely have diversified during the early Oligocene (Miralles et al 2015), giving rise to a dozen currently known species. In a recent study dealing with methodological aspects of species delimitation, Miralles and Vences (2013) applied and compared seven methods of delimitation to this genus, combining different approaches: (1) ITAX, the Integrative Taxonomic approach, which is based on the integration of as many lines of evidence as available to delimit species (cf.…”