[Herpetology • 2022] Slow and Steady wins the Race: Diversification Rate is Independent from Body Size and Lifestyle in Malagasy Skinks (Squamata: Scincidae: Scincinae)

 Malagasy Scincinae diversity
(A) Pseudoacontias menamainty, Berara. (B) Brachyseps macrocercus, Ankaratra. (D) Madascincus igneocaudatus, Ifaty.
(F) Amphiglossus astrolabi, Sainte Luce. (G) Voeltzkowia yamagishii, Ankarafantsika. (H) Voeltzkowia mira, Matsedroy.
(I) Paracontias vermisaurus, Makira. (K) Pygomeles braconnieri, near Ifaty. (L) Grandidierina sp. aff. rubrocaudata Andranomaitso.

in Belluardo, Muñoz-Pajares, Miralles, ... et Crottini, 2022.

 DOI: 10.1016/j.ympev.2022.107635 

 (photos: A - Franco Andreone; B - Frank Glaw and Miguel Vences; D, L - Gonçalo M. Rosa; F, H - Sam Hyde Roberts; G - Falk Eckhard; I - Miguel Vences; K - Aurélien Miralles)

Highlights: 

• A new species-level phylogenetic hypothesis and time-tree of the Malagasy Scincinae are provided.

• Diversification rate was constant until a sharp decrease around 6–4 million years ago.

• Body size evolved homogenously across sub-clades and did not influence diversification rate.

• Fossorial lifestyle evolved 5 independent times from quadrupedal ancestors and did not influence diversification rate.

• Diversification of fossorial sand-swimmer genera might be related to the aridification of Madagascar’s climate around 20 million years ago.

Abstract

Most of the unique and diverse vertebrate fauna that inhabits Madagascar derives from in situ diversification from colonisers that reached this continental island through overseas dispersal. The endemic Malagasy Scincinae lizards are amongst the most species-rich squamate groups on the island. They colonised all bioclimatic zones and display many ecomorphological adaptations to a fossorial (burrowing) lifestyle. Here we propose a new phylogenetic hypothesis for their diversification based on the largest taxon sampling so far for this group. We estimated divergence times and investigated several aspects of their diversification (diversification rate, body size and fossorial lifestyle evolution, and biogeography). We found that diversification rate was constant throughout most of the evolutionary history of the group, but decreased over the last 6–4 million years and independently from body size and fossorial lifestyle evolution. Fossoriality has evolved from fully quadrupedal ancestors at least five times independently, which demonstrates that even complex morphological syndromes – in this case involving traits such as limb regression, body elongation, modification of cephalic scalation, depigmentation, and eyes and ear-opening regression – can evolve repeatedly and independently given enough time and eco-evolutionary advantages. Initial diversification of the group likely occurred in forests, and the divergence of sand-swimmer genera around 20 Ma appears linked to a period of aridification. Our results show that the large phenotypic variability of Malagasy Scincinae has not influenced diversification rate and that their rich species diversity results from a constant accumulation of lineages through time. By compiling large geographic and trait-related datasets together with the computation of a new time tree for the group, our study contributes important insights on the diversification of Malagasy vertebrates.

 

Keywords: Biogeography, Evolutionary radiations, Fossoriality, In situ diversification, Islands, Madagascar

Fig. 1. An overview of the Malagasy Scincinae diversity.
 (A) Pseudoacontias menamainty, Berara. (B) Brachyseps macrocercus, Ankaratra. (C) Madascincus CaNew Betampona (of the Madascincus “nanus” group), Betampona. (D) Madascincus igneocaudatus, Ifaty.
 (E) Flexiseps ornaticeps, Ifaty. (F) Amphiglossus astrolabi, Sainte Luce. (G) Voeltzkowia yamagishii, Ankarafantsika. (H) Voeltzkowia mira, Matsedroy.
 (I) Paracontias vermisaurus, Makira. (J, K) Pygomeles braconnieri, near Ifaty. (L) Grandidierina sp. aff. rubrocaudata Andranomaitso.

 (Credits: A - Franco Andreone; B - Frank Glaw and Miguel Vences; C, D, E, L - Gonçalo M. Rosa; F, H - Sam Hyde Roberts; G - Falk Eckhard; I - Miguel Vences; J, K - Aurélien Miralles).

   

Francesco Belluardo, A .Jesus Muñoz-Pajares, Aurélien Miralles, Daniele Silvestro, Walter Cocca, Fanomezana Mihaja Ratsoavina, Andrea Villa, Sam Hyde Roberts, Marcello Mezzasalma, Alexander Zizka, Alexandre Antonelli and Angelica Crottini. 2022. Slow and Steady wins the Race: Diversification Rate is Independent from Body Size and Lifestyle in Malagasy Skinks (Squamata: Scincidae: Scincinae). Molecular Phylogenetics and Evolution. 107635, In Press. DOI: 10.1016/j.ympev.2022.107635