Thursday, January 28, 2021

[Herpetology • 2021] Brookesia nana • Extreme Miniaturization of A New Amniote Vertebrate and insights into the Evolution of Genital Size in Chameleons

Brookesia nana 
Glaw, Köhler, Hawlitschek, Ratsoavina, Rakotoarison, Scherz & Vences, 2021 

Evolutionary reduction of adult body size (miniaturization) has profound consequences for organismal biology and is an important subject of evolutionary research. Based on two individuals we describe a new, extremely miniaturized chameleon, which may be the world’s smallest reptile species. The male holotype of Brookesia nana sp. nov. has a snout–vent length of 13.5 mm (total length 21.6 mm) and has large, apparently fully developed hemipenes, making it apparently the smallest mature male amniote ever recorded. The female paratype measures 19.2 mm snout–vent length (total length 28.9 mm) and a micro-CT scan revealed developing eggs in the body cavity, likewise indicating sexual maturity. The new chameleon is only known from a degraded montane rainforest in northern Madagascar and might be threatened by extinction. Molecular phylogenetic analyses place it as sister to B. karchei, the largest species in the clade of miniaturized Brookesia species, for which we resurrect Evoluticauda Angel, 1942 as subgenus name. The genetic divergence of B. nana sp. nov. is rather strong (9.9‒14.9% to all other Evoluticauda species in the 16S rRNA gene). A comparative study of genital length in Malagasy chameleons revealed a tendency for the smallest chameleons to have the relatively largest hemipenes, which might be a consequence of a reversed sexual size dimorphism with males substantially smaller than females in the smallest species. The miniaturized males may need larger hemipenes to enable a better mechanical fit with female genitals during copulation. Comprehensive studies of female genitalia are needed to test this hypothesis and to better understand the evolution of genitalia in reptiles.

Brookesia nana sp. nov. in life. 
(A–C) male holotype (ZSM 1660/2012).
(D, E) female paratype (UADBA-R/FGZC 3752).

Molecular phylogeny of specimens in the subgenus Evoluticauda (known as Brookesia minima species group), based on the nuclear CMOS gene (alignment length 847 bp, but only about 400 bp available for all samples) and inferred under the Maximum Likelihood optimality criterion (K2P + G substitution model). Values at nodes are support values from a bootstrap analysis in percent (500 replicates) and are only shown if > 50%. The tree was rooted with B. brygooi (removed for better graphical representation).

Order Squamata Oppel, 181115.
Family Chamaeleonidae Rafinesque, 181516.
Subfamily Brookesiinae Angel, 194217.

Genus Brookesia Gray, 186517.

Subgenus Evoluticauda Angel, 1942 (resurrected herein, justification below).

Brookesia nana sp. nov
 Diagnosis: A diminutive chameleon species assigned to the genus Brookesia on the basis of its small body size, short tail, presence of rows of dorsolateral tubercles along vertebral column, presence of pelvic spine, and molecular phylogenetic relationships. Brookesia nana sp. nov. is distinguished by the following unique suite of morphological characters: (1) male SVL 13.5 mm, female SVL 19.2 mm; (2) male TL mm 21.6 mm, female TL 28.9 mm; (3) TaL/SVL ratio of 0.51 in male; (4) absence of lateral or dorsal spines on the tail; (5) absence of dorsal pelvic shield in sacral area; (6) presence of distinct pelvic spine; (7) pale brown dorsal colouration with slightly darker markings in life; (8) absence of apical spines on the hemipenis.

Etymology: The specific epithet is the Latin noun nana (meaning female dwarf) in the nominative singular.

Map of northern Madagascar, showing the distribution of species of the subgenus Evoluticauda (known as Brookesia minima group) in this region (only showing records verified by molecular data). Note that B. dentata, B. exarmata, and B. ramanantsoai occur further south and are not included in the map. Orange (dry forest) and green (rainforest) show remaining primary vegetation in 2003–2006.

Due to the old divergence and the morphological distinctness of the two clades we here suggest to consider them as different subgenera:

Subgenus Brookesia Gray, 1865 (large-bodied clade)
Type species: Chamaeleo superciliaris Kuhl, 1820.

Contents: Brookesia antakarana, B. bekolosy (attribution tentative), B. betschi, B. bonsi, B. brunoi, B. brygooi, B. decaryi, B. ebenaui, B. griveaudi, B. lambertoni, B. lineata, B. perarmata, B. stumpffi, B. superciliaris, B. therezieni, B. thieli, B. vadoni, B. valerieae.

Distribution: Madagascar.

Subgenus Evoluticauda Angel, 1942 (miniaturized clade, known as B. minima group)
Type species: Brookesia tuberculata Mocquard, 1894.

Contents: Brookesia confidens, B. dentata, B. desperata, B. exarmata, B. karchei, B. micra, B. minima, B. nana, B. peyrierasi, B. ramanantsoai, B. tedi, B. tristis, B. tuberculata.

Distribution: Northern half of Madagascar.

Frank Glaw, Jörn Köhler, Oliver Hawlitschek, Fanomezana M. Ratsoavina, Andolalao Rakotoarison, Mark D. Scherz and Miguel Vences. 2021. Extreme Miniaturization of A New Amniote Vertebrate and insights into the Evolution of Genital Size in Chameleons. Scientific Reports. 11, 2522. DOI: 10.1038/s41598-020-80955-1