Making a bat: The developmental basis of bat evolution

Abstract

Bats are incredibly diverse, both morphologically and taxonomically. Bats are the only mammalian group to have achieved powered flight, an adaptation that is hypothesized to have allowed them to colonize various and diverse ecological niches. However, the lack of fossils capturing the transition from terrestrial mammal to volant chiropteran has obscured much of our understanding of bat evolution. Over the last 20 years, the emergence of evo-devo in non-model species has started to fill this gap by uncovering some developmental mechanisms at the origin of bat diversification. In this review, we highlight key aspects of studies that have used bats as a model for morphological adaptations, diversification during adaptive radiations, and morphological novelty. To do so, we review current and ongoing studies on bat evolution. We first investigate morphological specialization by reviewing current knowledge about wing and face evolution. Then, we explore the mechanisms behind adaptive diversification in various ecological contexts using vision and dentition. Finally, we highlight the emerging work into morphological novelties using bat wing membranes.

Figure 1 -. Phylogeny of bats. (a) Cladogram* showing intraordinal phylogenetic relationships in Chiroptera (adapted from Teeling et al., 2018). Based on molecular data, Chiroptera is now classified into Yinpterochiroptera (orange) and Yangochiroptera (magenta), while the traditional classification into microbats and megabats is shown in grey. (b) Cladogram* showing the interordinal relationship between Chiroptera and other mammalian taxa (adapted from Jebb et al., 2020). Three of the best supported tree topologies for the relationship between the Laurasiatherian lineages Carnivora, Perrissodactyla, Cetartiodactyla, Pholidota and Chiroptera (indicated by shaded area) are shown. *Branch lengths do not indicate distance.

Figure 2 -. Differences in signaling centers between bat and mouse limb development. Larger expression domains in bat AER and ZPA, combined with a feedback loop caused by later re-initiation of Fgf8 and Shh, contributes to lengthening in bat forelimbs (reproduced from Cooper and Sears, 2013).

Figure 3 -. Color vision diversity in Phyllostomids (adapted from Sadier et al., 2018). Cones are shown on flat-mounted retinas in four different bat species representative of the cone diversity in Phyllostomids. To visualize L opsin (green) and S opsin (magenta), flat-mounted retinas were probed with two antibodies against L and S opsins. L opsin expressing cones were found in all bats, while S opsins were only seen in fruit visiting Carollia and Artibeus species, indicating cone type and diversity vary between species occupying different dietary niches. Diet is indicated with a pictogram.

Figure 4 -. Jaw and dental diversity of Noctilionoid bats. Members of the group occupy every possible dietary niche found in bats. In line with this, jaw size and shape as well as tooth shape, size and proportion are highly variable in Noctilionoid bats. In fact, the jaw and tooth types shown represent most of the breadth of the diversity found in both bat superfamilies. Diet is indicated with a pictogram. Scale: 10 mm

Figure 5 -. The anatomy and development of the bat wing (a) Outline of extended forelimb and wing membranes in chiropterans demonstrating the skeleton and membranes (patagia) of the wing (from Swartz et al., 1996). (b) Examples of variation in size and shape of patagia (from Norberg and Rayner, 1987). (c) Early limb development in bats compared to mice showing early similarities in limb development and divergence in growth and maturation. (from Cretekos et al., 2008).