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. 2024 Jul 25:12:e17824.
doi: 10.7717/peerj.17824. eCollection 2024.

Gliding toward an understanding of the origin of flight in bats

Abigail E Burtner  1 , David M Grossnickle  1   2 , Sharlene E Santana  1 , Chris J Law  1   3
Affiliations

Gliding toward an understanding of the origin of flight in bats

Abigail E Burtner et al. PeerJ. .

Abstract

Bats are the only mammals capable of powered flight and have correspondingly specialized body plans, particularly in their limb morphology. The origin of bat flight is still not fully understood due to an uninformative fossil record but, from the perspective of a functional transition, it is widely hypothesized that bats evolved from gliding ancestors. Here, we test predictions of the gliding-to-flying hypothesis of the origin of bat flight by using phylogenetic comparative methods to model the evolution of forelimb and hindlimb traits on a dataset spanning four extinct bats and 231 extant mammals with diverse locomotor modes. Our results reveal that gliders exhibit adaptive trait optima (1) toward relatively elongate forelimbs that are intermediate between those of bats and non-gliding arborealists, and (2) toward relatively narrower but not longer hindlimbs that are intermediate between those of non-gliders and bats. We propose an adaptive landscape based on limb length and width optimal trends derived from our modeling analyses. Our results support a hypothetical evolutionary pathway wherein glider-like postcranial morphology precedes a bat-like morphology adapted to powered-flight, setting a foundation for future developmental, biomechanical, and evolutionary research to test this idea.

Keywords: Adaptive landscape; Ecomorphology; Macroevolution; Ornstein–Uhlenbeck modeling; Phylogenetic comparative methods.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1
Figure 1. Morphological measurements and phylogeny.
We conducted analyses based on the mammalian phylogeny from Upham, Esselstyn & Jetz (2019) across 14 forelimb linear measurements and 15 hindlimb measurements for each specimen. The forelimb measurement consisted of scapula height and length (sh, sl), humerus length (hl), distal width (hdw), proximal width (hpw), and mid-shaft width (hsw), radius length (rl), ulna length and olecranon length (ul, uol), and third manual digit metacarpal length and width (mcl, mcw), proximal phalanx length and width (ppl, ppw), and intermediate phalanx length (ipl). The hindlimb measurements consisted of pelvis, ilium, and ischium length (pel, il, isl); femur length (fl), distal width (fdw), and midshaft width (fsw); tibia length (tl), proximal length (tpw), and midshaft width (tmw); fibula length (fbl), and third pedal digit metatarsal length and width (mtl, mtw), proximal phalanx length and width (ppxl, ppxw), and intermediate phalanx length (ipxl). We measured only the third digit in this dataset (and not, for example, the fifth even though that might be of biological interest) to build on previous datasets in the literature to generate a large enough dataset for evolutionary modeling. The skeletal figures are modified from Chen & Wilson (2015).
Figure 2
Figure 2. Forelimb and hind limb PCAs.
Morphospaces consist of PC1 and PC2 of 14 forelimb traits (left panels) and 15 hind limb traits (right panels). The extant+extinct morphospace is shown for the (A) forelimbs and (B) hind limbs. The extant-only morphospace of (C) the mvOUMloc3b optima (large icons) overlaid on the forelimb morphospace and the (D) the mvOUMloc4 optima (large icons) overlaid on the hind limb morphospace. Cartoons of a (E) quadrupedal mammal skeleton (Rattus norvegicus) versus a (F) bat skeleton (Pipistrellus abramus) are shown where dark gray shaded bones on the cartoon skeletons correspond to those measured to generate the morphospace.
Figure 3
Figure 3. (A–J) Forelimb trait optima from model-fitting of univariate traits.
Forelimb OUM optima (θ) as a size-corrected trait value (log-shape ratio) with 95% confidence intervals (Tables S3a) for the best-fitting models (ΔAIC = 0) for 10 traits. The AICcW of the model is on top of each panel (Table S2a).
Figure 4
Figure 4. (A–J) Hind limb trait optima from model-fitting of univariate traits.
Hind limb OUM optima (θ) as a size-corrected trait value (log-shape ratio) with 95% confidence intervals (Tables S3b) for the best-fitting models (ΔAIC = 0) for 10 traits. The AICcW of the model is on top of each panel (Table S2b).
Figure 5
Figure 5. (A and B) Clade-specific evolutionary shifts in limb morphology across the mammalian phylogeny identified by PhylogeneticEM.
Shifts are represented as colored circles, and branches on the phylogenies are colored according to each regime.
Figure 6
Figure 6. Hypothetical adaptive landscapes of forelimb and hind limb skeletal relative length and width evolution.
Hypothetical fitness peaks are shown for arborealists, gliders, and bats for a broad summary of our conclusions from the skeletal trait optima results discussed. The “length” and “width” in the figure refer to the lengths and widths of individual limb elements. For the (A) forelimb, we depict arborealists on a relatively steep adaptive peak at relatively lower length/width optima, gliders on a broad, shallow peak/incline at relatively higher length but not width optima, and bats on a very steep peak at relatively higher length and width optima. For the (B) hind limb, we depict arborealists again on a fairly steep adaptive peak at relatively higher width but not length optima, bats on a shallow steep peak at relatively higher length and lower width optima, and gliders on a peak similar to and overlapping with bats’ at relatively higher length but similar width optima.
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