Skull evolution and lineage diversification in endemic Malagasy carnivorans

Abstract

Madagascar is one of the world's foremost biodiversity hotspots with more than 90% of its species endemic to the island. Malagasy carnivorans are one of only four extant terrestrial mammalian clades endemic to Madagascar. Although there are only eight extant species, these carnivorans exhibit remarkable phenotypic and ecological diversity that is often hypothesized to have diversified through an adaptive radiation. Here, we investigated the evolution of skull diversity in Malagasy carnivorans and tested if they exhibited characteristics of convergence and an adaptive radiation. We found that their skull disparity exceeds that of any other feliform family, as their skulls vary widely and strikingly capture a large amount of the morphological variation found across all feliforms. We also found evidence of shared adaptive zones in cranial shape between euplerid subclades and felids, herpestids and viverrids. Lastly, contrary to predictions of adaptive radiation, we found that Malagasy carnivorans do not exhibit rapid lineage diversification and only marginally faster rates of mandibular shape evolution and to a lesser extent cranial shape evolution, compared to other feliforms. These results reveal that exceptional diversification rates are not necessary to generate the striking phenotypic diversity that evolved in carnivorans after their dispersal to and isolation on Madagascar.

Keywords: Carnivora; Madagascar; adaptive radiation; craniomandibular; phenotypic evolution; phylogenetic comparative methods.

Figure 1.

Phylogeny of Eupleridae and other extant feliform Carnivora families. Phylogeny based on [33]. Oligo, Oligocene; Ple, Pleistocene; Pli, Pliocene.

Figure 2.

Morphospace of allometry-free cranial (left) and mandibular (right) shape defined by PC axes 1−3. Taxa illustrated for the cranial morphospace: (a) bBrown hyena (Hyaena brunnea (Hyaenidae)), –PC 1; (b) Javan mongoose (Urva javanicus (Herpestidae)), +PC 1; (c) Pallas’s cat (Otocolobus manul (Felidae)), +PC 2; (d) eastern falanouc (E. goudotii (Eupleridae)), –PC 2; (e) Asian palm civet (Paradoxurus hermaphroditus (Eupleridae)), +PC 3; and (f) Egyptian mongoose (Herpestes ichneumon (Herpestidae)), –PC 3. Taxa illustrated for the mandibular morphospace: (g) tiger (Panthera tigris (Felidae)), –PC 1; (h) small Indian civet (Viverricula indica (Viverridae)), +PC 1; (i) Ethiopian dwarf mongoose (Helogale hirtula (Herpestidae)), +PC 2; (j) eastern falanouc (E. goudotii (Eupleridae)), –PC 2; (k) large Indian civet (Viverra zibetha (Viverridae)), +PC 3; and (l) binturong (Arctictis binturong (Viverridae)), –PC 3. Grey circles indicate estimated ancestral shapes at nodes, and the green star indicates estimated ancestral shape of the ancestral euplerid node.

Figure 3.

Phylorate plots of cranial and mandibular shape evolutionary rates across feliform Carnivora. Warmer colours indicate faster rates and cooler colours indicate slower rates. Significant shifts in evolutionary rate are shown as grey circles with sizes proportional to the posterior probability. All rates were log-transformed.

Figure 4.

Phylorate plot of lineage diversification rates across feliform Carnivora using BAMM. Colours at each point in time along the branches of the phylorate plot denote instantaneous rate of diversification. Warmer colours indicate faster rates and cooler colours indicate slower rates. There are no significant shifts in diversification rates across the phylogeny. Analyses of lineage diversification rates using LSBDS resulted in similar patterns (electronic supplementary material, figure S2).

Figure 5.

Thin-plate spline deformation grids depicting cranial shape differences between euplerid clades and other feliform families. (a) Cranial shape of the fossa (C. ferox) appears intermediate between felids and other euplerids. (b) Cranial shape of euplerines: the fanaloka (F. fossana) resembles viverrids, whereas the eastern falanouc (E. goudotii) exhibits a more specialized morphology. (c) Cranial shapes of most galidiines resemble herpestids.

Figure 6.

Thin-plate spline deformation grids depicting mandibular shape differences euplerid clades and other feliform families. (a) Mandibular shape of the fossa (C. ferox) appears intermediate between felids and euplerids. (b) Mandibular shape of euplerines: the fanaloka (F. fossana) resemble viverrids, whereas the eastern falanouc (E. goudotii) exhibits a more specialized morphology. (c) Mandibular shapes of most galidiines resemble herpestids, although the mandibular shape (d) of Grandidier’s vontsira (G. grandidieri) appears intermediate between felids and other galidiines.