Taxonomic allocation of KNM-RU 18340

Rieppel et al.14 only wrote a preliminary report on the KNM-RU 18340 specimen as their study was based only on a cast and on photographs of the original material. These authors suggested that this fossil may potentionally be an early representative of the genus Rhampholeon, although as acknowledged by them, no living species of the genus Rhampholeon shows a fully separated prefrontal fenestra (called “prefrontal fontanelle” in their report) - they claimed (erroneously as we know now) the complete separation of external nares from the prefrontal fenestra in KNM-RU 18340.

Thanks to micro-computed tomography (μCT), we were able to identify all skull bones and observe their internal sides as well as their sutures. Moreover, the micro-CT revealed elements that are hidden by the rocky matrix and could not be studied before, such as an almost complete braincase with stapes, the palate region, a ceratohyal and the first three cervical vertebrae (Fig. 2, Supplementary Data 1).

The morphological comparisons are in agreement with the results of the phylogenetic analyses that specimen KNM-RU 18340 can be distinguished from all extant genera, except from Calumma. Overall the morphology of the fossil skull most closely resembles that seen in the extant Ca. brevicorne (see Fig. 3d–f), especially the shape of the parietal, the arrangement of protuberances on the parietal, the dorsal opening of the supratemporal fenestra (not visible in lateral aspect; this is also present in Ca. parsonii, Ca. globifer and Ca. ambreense), the presence of the prefrontal-postorbitofrontal contact over the orbit and the maximum width of the skull being located at the level of the frontal-parietal contact in dorsal view (the maximum width in Ca. parsonii, Ca. globifer and Ca. ambreense is posterior to this region, in the mid-section of upper temporal fenestra). But there are also some differences, e.g. the absence of the premaxilla-frontal contact, the separation of the external naris from the prefrontal fenestra, and the straight orbital margin in dorsal view in the extant species (see above).

The preserved elements of KNM-RU 18340 possess a unique combination of character states (see Diagnosis), and a new taxon name is therefore erected: Calumma benovskyi sp. nov. There is also one unique character: well defined and laterally expanded triangular posterolateral processes of the frontal. Although in some species of Calumma (e.g., Ca. nasutum and Ca. vatosoa)24,26 the posterolateral corners of the frontal expand laterally, they do not form a well-defined triangular processes as present in the early Miocene Ca. benovskyi sp. nov. The processes are not developed in Brookesia and Palleon, but are well-expanded laterally in the outgroup taxon Uromastyx.

Biogeographic history of malagasy chameleons

Our results show that KNM-RU 18340 represents the first evidence of a member of the Calumma lineage on continental Africa. The extant species of this genus (together with the Brookesiinae, see; Fig. 3b here) are endemic to the island of Madagascar (Furcifer is distributed on Madagascar, but there are two species on the Comoros as well)4,34, which harbours an exceptional biodiversity. The separation of this island from Africa occurred already in the early Cretaceous35. Although the presence of a Malagasy lineage in continental Africa during the early Miocene might appear as a surprise, similar patterns have been observed for Madagascar’s endemic terrestrial extant mammals. Based on phylogenetic analyses, tenrecs36,37, euplerid carnivores36,38 and nesomyine rodents36 appear to be monophyletic taxa, whose sister group is found in Africa. They each result from a single colonization event and subsequent radiation within the island39. Likewise, recent palaeontological discoveries suggest that two lemur lineages likely dispersed from Africa to Madagascar across the Mozambique Channel independently, and thus have an African origin36,40. The dispersal window for these four endemic clades is estimated to span from the Oligocene to the early Miocene36,40. It is also worth noting that some other squamate lineages such as pythons and varanids did not manage to follow this dispersal route.

The origin of chameleons?

Raxworthy et al.3 suggested that chameleons originated on Madagascar and dispersed over water at least three times to Africa, and once each to the Seychelles, to the Comoros archipelago (where they occupy two islands) and to Reunion. In contrast, Tolley et al.4 suggested that the family originated in Africa, with two separate oceanic dispersal events to Madagascar during the Palaeocene (Brookesiinae lineage) and the Oligocene, when prevailing oceanic currents would have favoured eastward dispersal. The early Miocene Calumma benovskyi sp. nov. supports an African continental origin for Malagasy chamaeleonine lineages, at least for the Calumma clade. The oceanic dispersal using currents that favoured eastward dispersal appears to be the most probable scenario (Fig. 3g). The existence of such eastward currents from the African shore to Madagascar between the Palaeocene and the early Miocene is well documented41,42. Lizards such as chameleons might have used floating islands—rafts of trees (this is especially plausible for arboreal lizards) —to cross such distances43. Rafting has been suggested for anole lizards migrating around the Caribbean44 or for mabuyid skink Trachylepis atlantica on the island of Fernando de Noronha (Brazil), where the ancestors of this species are believed to have rafted from Africa, across the Atlantic, during the last 9 million years45; Trachylepis is otherwise distributed in Africa and Madagascar46.

The African origin of Calumma is also supported by the distribution of members forming a clade [Chamaeleo + Trioceros + Kinyongia + Furcifer + Calumma]; where only the latter two taxa are found in Madagascar4. According to Tolley et al.4, Calumma and Furcifer are sister taxa and the split of these two lineages occured in the Eocene. But within these genera, species-level divergence occured during the Oligocene and Miocene. However, if the split is older than the documented early Miocene occurrence of the extinct continental species Ca. benovskyi sp. nov., this might suggest that the last common ancestor of these two lineages most likely lived on the continent. This then suggests a continental origin for both, Calumma and Furcifer.

Although the Miocene Calumma benovskyi sp. nov. represents the oldest known member of this genus and shares some characters with the basal node of this clade, based on our current knowledge we can assume that Ca. beniovskyi most likely does not form an ancestral lineage for the Calumma clade. It is recovered as sister to Ca. brevicorne rather than in a basal position to all Calumma. Moreover, molecular data suggest that the ancestral lineage should be older than the early Miocene4; yet, this remains to be verified with fossil data of an older age. For now the diversity and morphological disparity of the Oligocene and early Miocene Calumma in Africa remains unknown. However, the assignment of KNM-RU 18340 to the genus Calumma and its presence in the early Miocene of Kenya demonstrates that the Calumma lineage was present in Africa at a time when oceanic currents supported eastward dispersal41,42. This is consistent with the previously suggested hypothesis of Tolley et al.4 based on molecular data.

Is the alternative scenario possible?

The above scenario challenges a dispersal of the genus Calumma from Madagascar to Africa through oceanic dispersal, as previously suggested by Raxworthy et al.3. According to several authors (e.g., Ali and Huber41, Samonds et al.42), the prevailing oceanic currents at that time support dispersal from Africa to Madagascar, and not the other way around. According to McCall47, some areas of the Mozambique Channel were dry land during the middle Eocene - early Miocene. Even if animals used several intervening islands in a stepping-stone chain, eastward currents would have hindered their westward dispersal. Moreover, chameleons are relatively poor swimmers rendering the westward route scenario even less probable. Ali and Huber41 also pointed out that shortly after the early Miocene, the currents between Africa and Madagascar turned in the opposite direction (i.e. westwards, toward Africa), like in present-day surface-water circulation. From the middle Miocene onwards, currents would thus have hindered journey to Madagascar for any non-volant and non-swimming taxa, and could have supported the development of insular endemism for terrestrial animals there.

Hence, the “out of Madagascar” dispersal scenario would have required the existence of fully terrestrial land bridge between the late Oligocene and the early Miocene. Of note is that the separation of Africa and Madagascar occurred already during the Mesozoic35. But such a bridge would have enabled any taxon, even large animals (e.g., elephants), to disperse. This scenario would neither explain the quasi absence of large-bodied terrestrial mammals, nor the limited number of mammal families that live on the island today.