Chiroptera

Chiroptera (from the Ancient Greek cheir, "hand," and pteron, "wing") is the order of placental mammals (Laurasiatheria, Mammalia) comprising all bats. With more than 1,460 described extant species across 21 families, Chiroptera is the second-largest order of mammals (after Rodentia), accounting for more than 20% of all living mammalian species on Earth. Bats are the only mammals ever to evolve sustained, true powered flight (as opposed to passive gliding in colugos, flying squirrels, and sugar gliders), enabling them to colonize every continent except Antarctica and serve as essential nocturnal insect predators, tropical seed dispersers, and chiropterophilous nectar pollinators (for agaves, baobabs, durians, and columnar cacti).

Within the Boreoeutherian superorder Laurasiatheria, phylogenomic analyses place Chiroptera inside Scrotifera alongside Ferae (Carnivora + Pholidota) and Euungulata (Perissodactyla + Cetartiodactyla). Already present as fully winged flyers by the Early Eocene (~52.5 million years ago) in the Green River Formation of Wyoming (Onychonycteris finneyi and Icaronycteris index) and the Messel Pit of Germany, bats underwent a rapid global radiation across nocturnal aerial niches.

1. The Compliant Multi-Jointed Hand-Wing (Patagium) and BMP2 Finger Elongation: Whereas birds fused their wrist and finger bones into a rigid rod supporting stiff β-keratin feathers and pterosaurs stretched a fibrous wing along a single hypertrophied fourth finger, the bat wing is a modified five-fingered mammalian hand:
   • The thumb (pollex, digit I) remains short, free, and armed with a curved claw for climbing;
   • The second through fifth metacarpals and phalanges (digits II, III, IV, and V) are elongated by 300% to 500%—driven during embryonic development by a 30% surge in Bone Morphogenetic Protein 2 (Bmp2) expression inside hypertrophic growth-plate chondrocytes (Sears et al., 2006) paired with heightened Fgf8 and Shh feedback loops that block interdigital apoptosis (Weatherbee et al., 2006).
   • Stretched across these four flexible fingers, the arm, the flank, and the hindlegs is a living, two-layered skin membrane—the patagium (subdivided into the leading-edge propatagium, inter-digital dactylopatagium, flank plagiopatagium, and tail uropatagium). As shown by Sharon M. Swartz and Kenneth S. Breuer, bat wing bones are poorly mineralized and remarkably flexible, while the patagium contains an array of microscopic intrinsic striated muscles (plagiopatagialis), elastin bundles, and Merkel-cell-associated sensory hairs that sense boundary-layer airflow separation and actively adjust wing camber across >25 independent skeletal degrees of freedom—enabling bats to execute tighter, higher-lift slow-speed maneuvers and leading-edge vortices than birds!
2. 180° Hindlimb Rotation and the Passive Digital Tendon-Locking Mechanism: Bat hip joints are rotated 90°–180° outward and backward so the knees point dorsolaterally, optimized for hanging upside-down by the hindfeet rather than upright walking (with the notable exception of Neotropical vampire bats, Desmodus rotundus, and the New Zealand lesser short-tailed bat, Mystacina tuberculata, which bound rapidly on the ground using folded wrist thumbs!). How does a bat hang upside-down while sleeping—or even after dying—without expending any muscular energy? As elucidated by W. A. Schutt Jr. and colleagues (1993), the flexor digitorum tendon of each toe carries microscopic scaly tubercles on its ventral surface that slide into a ridged fibrous tendon sheath (retinaculum) when the weight of the bat's hanging body pulls the tendon taut—functioning like a mechanical zip-tie ratchet that locks the claws shut around a cave ceiling or branch with zero ATP expenditure until the bat flexes its ankle to disengage the lock!

For over a century, anatomists divided bats into two suborders based on size, diet, and echolocation: Megachiroptera ("megabats": large, fruit-eating Old World flying foxes that lack laryngeal echolocation) versus Microchiroptera ("microbats": all small, laryngeal-echolocating bats). In 2001–2005, nuclear phylogenomics by Emma C. Teeling, Mark S. Springer, Stephen J. Rossiter, and colleagues overturned this classification: five families of laryngeal-echolocating "microbats" (including horseshoe bats, leaf-nosed bats, and false vampires) are actually closer relatives of non-echolocating Old World fruit bats than of other microbats!

Despite weighing only 5 to 10 grams and having metabolic rates during flight 15 to 16 times their basal rate (reaching 3× the mass-specific metabolic rate of a running mammal of equal size and core temperatures of 40–41 °C), bats such as Brandt's myotis (Myotis brandtii, 4–8 g) live over 41 years in the wild (~9–10 times longer than predicted for their body mass, Podlutsky et al., 2005) and asymptomatically harbor zoonotic RNA and DNA viruses (rabies/lyssaviruses, coronaviruses, filoviruses, and henipaviruses) without falling ill. Comparative genomics by Guojie Zhang, Lin-Fa Wang, Emma C. Teeling, Sonja C. Vernes, and colleagues (2013, 2018, 2020) revealed how the evolution of powered flight reshaped bat innate immunity and aging:

1. Dampened Cytosolic DNA Sensing (Loss of the PYHIN Gene Family and Attenuated STING): During high-energy flight, mitochondrial reactive oxygen species (ROS) damage nuclear and mitochondrial DNA, leaking self-DNA fragments into the cytosol. In humans or mice, cytosolic DNA triggers AIM2 (PYHIN) inflammasomes and cGAS–STING to unleash a lethal inflammatory cytokine storm. To survive daily flight-induced DNA leakage, bats deleted the entire PYHIN (AIM2 / IFI16) inflammasome gene family, mutated the conserved Ser358 phosphorylation site of STING to dampen downstream IFN-β over-activation (Xie et al., 2018), and dampened NLRP3 inflammasome activation (Ahn et al., 2019)!
2. Constitutive Baseline Interferon-α (IFN-α) Expression and Positively Selected DNA Repair: To compensate for dampened inflammatory pathology without succumbing to infections, bats (Pteropus alecto) maintain constitutively active baseline levels of antiviral Interferon-α (IFN-α) even in unstimulated cells (Zhou et al., 2016), while positive selection on ATM, PRKDC (DNA-PKcs), RAD50, KU80, and TP53 repairs oxidative DNA double-strand breaks and maintains telomere length across four decades of life without shortening (Foley et al., 2018).

What does the Early Eocene fossil Onychonycteris finneyi ("clawed bat") reveal about which evolved first: flight or echolocation?

For decades, evolutionary biologists debated three hypotheses for the origin of bats: (1) "flight first," (2) "echolocation first" (in nocturnal insectivorous shrews/gliders), or (3) "tandem co-evolution." In 2008, Nancy B. Simmons, Kevin L. Seymour, Jörg Habersetzer, and Gregg F. Gunnell described two complete skeletons of Onychonycteris finneyi from the 52.5-million-year-old Green River Formation of Wyoming. Onychonycteris possessed intermediate limb proportions between non-flying climbers and later bats, retained claws on all five wing fingers (modern bats have claws on only one or two fingers), and had fully functional wings capable of undulating flutter-and-glide flight—yet micro-CT scans of its inner ear and stylohyal throat bones showed a small, unexpanded cochlea and non-articulated stylohyal, proving definitively that powered flight evolved before laryngeal ultrasonic echolocation!

What is White-Nose Syndrome (Pseudogymnoascus destructans) and why has it devastated North American hibernating bats?

Since its introduction to a cave near Albany, New York in 2006, the psychrophilic (cold-loving, optimal growth at 12–16 °C, dead above 20 °C) Eurasian ascomycete fungus Pseudogymnoascus destructans (Pd) has killed millions of hibernating North American cave bats (causing >90% declines in little brown bats (Myotis lucifugus), northern long-eared bats, and tricolored bats). Rather than attacking internal organs, Pd invades the living epidermis and sebaceous glands of the wing membranes (patagium) while the bat's body temperature is dropped to ambient cave temperatures (2–10 °C) and immune activity is suppressed during hibernation torpor. Epidermal erosion causes severe transcutaneous water and electrolyte loss, forcing infected bats to arouse from torpor 3 to 4 times too frequently, burning through their entire winter brown-adipose fat reserves before spring arrives (Warnecke et al., 2012).

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2. Sears, K. E., Behringer, R. R., Rasweiler, J. J., IV, & Niswander, L. A. (2006). Development of bat flight: Morphologic and molecular evolution of bat wing digits. Proceedings of the National Academy of Sciences, 103(17), 6581–6586. doi:10.1073/pnas.0509716103
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6. Jebb, D., Huang, Z., Pippel, M., Hughes, G. M., Lavrichenko, K., Devanna, P., ... & Teeling, E. C. (2020). Six reference-quality genomes reveal evolution of bat adaptations. Nature, 583(7817), 578–584. doi:10.1038/s41586-020-2486-3