Signatures of echolocation and dietary ecology in the adaptive evolution of skull shape in bats

Abstract

Morphological diversity may arise rapidly as a result of adaptation to novel ecological opportunities, but early bursts of trait evolution are rarely observed. Rather, models of discrete shifts between adaptive zones may better explain macroevolutionary dynamics across radiations. To investigate which of these processes underlie exceptional levels of morphological diversity during ecological diversification, we use modern phylogenetic tools and 3D geometric morphometric datasets to examine adaptive zone shifts in bat skull shape. Here we report that, while disparity was established early, bat skull evolution is best described by multiple adaptive zone shifts. Shifts are partially decoupled between the cranium and mandible, with cranial evolution more strongly driven by echolocation than diet. Phyllostomidae, a trophic adaptive radiation, exhibits more adaptive zone shifts than all other families combined. This pattern was potentially driven by ecological opportunity and facilitated by a shift to intermediate cranial shapes compared to oral-emitters and other nasal emitters.

Fig. 1

Cranial and mandibular morphospaces of bats based on phylogenetic PCA. Digital models of crania and mandibles from μCT data illustrate the trends across each axis, 3D models visualized using Checkpoint. Taxa illustrated: Cranium (a, b) —pPC1 (+Centurio senex, −Macroglossus sobrinus), pPC2 (+Mormoops blainvillei, −Hipposideros caffer), pPC3 (+Tylonycteris robustula, − Lophostoma silvicolum); Mandible (c, d) —pPC1 (+Choeronycteris mexicanus, −Centurio senex), pPC2 (+Myzopoda aurita, −Dobsonia praedatrix), pPC3 (+Macroglossus sobrinus, −Mormoops megalophylla), pPC4 (+Desmodus rotundus, −Megaderma spasma). Percent values give the R² from a Procrustes multiple regression of landmark coordinates on pPC scores, see Methods and source data file

Fig. 2

Disparity-through-time plots for the shape of the cranium and mandible across bats. Thick black line = observed subclade disparity. Gray polygon = area of 95% confidence interval of BM simulated character histories. Dashed line = medium DTT curve of BM simulated character histories. See source data file

Fig. 3

Tanglegrams of phylogenetic relationships of Chiroptera, and morphology dendrograms of bat skull shape. a cranium, b mandible. Dotted lines link the same species in both trees

Fig. 4

Evolutionary shifts (asterisks) in cranium shape across bats. Shifts were determined by l1ou adaptive landscape model fitting on pPCA scores using pBIC (pPC 1–3; Fig. 1). Bootstrap support is given for shift locations. Blue shifts = transition in echolocation type, Red shifts = transitions in diet, Purple shifts = transition in echolocation type and diet, Black shifts = no transition. Digital models of crania from μCT data illustrate the sample taxa from each adaptive regime, 3D models were visualized using Checkpoint. Representative taxa, from top to bottom: Pteropus poliocephalus, Hipposideros caffer, Nycteris hispida, Mormoops blainvillei, Desmodus rotundus, Choeronycteris mexicana, Phylloderma stenops, Ametrida centurio, Centurio senex, Corynorhinus townsendii, Murina leucogaster. Yin. = Yinpterochiroptera. Yang. = Yangochiroptera

Fig. 5

Evolutionary shifts (asterisks) in mandible shape across bats. Shifts were determined by l1ou adaptive landscape model fitting on pPCA scores using pBIC (pPC 1–4; Fig. 1). Bootstrap support is given for shift locations. Blue shifts = transition in echolocation type, Red shifts = transitions in diet, Purple shifts = transition in echolocation type and diet, Black shifts = no transition. Representative taxa from well-supported shifts, from top to bottom; Left: Rousettus aegyptiacus, Myotis lucifugus, Desmodus rotundus, Anoura geoffroyi, Lonchophylla robusta, Chiroderma villosum; Right: Syconycteris australis, Noctilio leporinus, Choeronycteris mexicana, Rhinophylla pumilio, Sphaeronycteris toxophyllum, Tylonycteris robustula. Yin. = Yinpterochiroptera. Yang. = Yangochiroptera

Fig. 6

Adaptive shifts in cranial and mandibular morphospaces (pPC scores). Digital models of crania and mandibles from μCT data illustrate the trends across each axis, 3D models were visualized using Checkpoint. Illustrated taxa as in Fig. 1. Polygons indicate pPC score distributions of all species representing an adaptive evolutionary regime shift for the cranium (a, b) or mandible (c, d) with at least 0.7 bootstrap support. Arrows indicate the transition between ancestral adaptive regime (gray polygon) and the new adaptive regime for each evolutionary shift. Colors of adaptive regimes match those illustrated in Figs. 4 and 5. See source data file