9/24 Locomotion: Fossorial, Gliding, and Flying

Fossorial and Semi-Fossorial Taxa: Ecosystem Engineers and Keystone Species

• Prairie Dogs as Ecological Influencers: Prairie dogs serve as both ecosystem engineers and keystone species.
  • Ecosystem Engineers: They physically modify their environment through burrowing, which creates habitat and alters soil composition. These physical changes have significant ecological effects.
  • Keystone Species: Beyond their engineering role, their presence has a profound ecological impact disproportionate to their biomass, making them keystone species. This impact isn't solely through physical modification.
• Trophic Roles:
  • They act as herbivores, consuming plant material.
  • They serve as prey items for various predators, including coyotes and foxes.
• Ecological Impact Visuals (Conceptual):
  • Trophic lines (e.g., predator-prey relationships) are depicted as solid connections.
  • Ecosystem engineering lines (e.g., physical environmental modification) are shown as dashed connections.
• Positive Ecological Effects of Prairie Dog Mounds: The presence of prairie dog mounds contributes to a variety of positive ecological outcomes, indicated in red in the original context.
  • Increased predator populations.
  • Support for megaherbivores like buffaloes.
  • More pollinators.
  • Enhanced habitat for other taxa.
  • Increased abundance of flowers.
• Ecological Heterogeneity: Prairie dogs create ecological heterogeneity (varied environments) across multiple spatial scales:
  • Single mound scale: They alter the immediate area, leading to more flowers, pollinators, and small organisms living in burrows.
  • Colony scale: As they are colonial, this effect scales up to larger areas (e.g., a football field-sized colony).
  • Largest scale: Different colonies contribute to heterogeneity across vast landscapes.
• Global Convergence: Grasslands worldwide feature fossorial and semi-fossorial taxa that play similar crucial ecological roles through convergent evolution.
  • North America: Examples include prairie dogs, squirrels, marmots, and pikas (which are rabbits, not rodents).
  • Australia: Various marsupials fulfill these roles.
  • All these taxa are burrowing, either as fossorial or semi-fossorial organisms.
• Persecution and Habitat Conversion: These taxa are often persecuted because their grassland habitats are highly desirable for human agriculture. Efforts are made to remove them, leading to habitat conversion (e.g., the Great Plains of North America have been largely converted).

Locomotion: Gliding

• Introduction to Gliding: Gliding is a mode of locomotion distinct from flying; it is important to note that flying did not evolve from gliding.

• Characteristics of Gliders:

  • Arboreal Lifestyle: Gliders are always arboreal, living in trees, as they require height to initiate a glide (starting high to go down).
  • Nocturnality: Interestingly, gliders are almost universally nocturnal, which seems paradoxical given that gliding can be dangerous.

• Evolutionary History of Gliding:

  • Gliding has evolved at least nine times in extinct taxa.
  • It has evolved at least six times in living mammals, encompassing approximately $100$ species.
  • In mammals, it evolved:
    • Three times in Diprotodon marsupials (e.g., the sugar glider).
    • At least twice (possibly more) in rodents (e.g., flying squirrels, which include $14$ gliding genera. The monophyly of these 14 genera as a single clade is still debated, so gliding might have evolved multiple times within squirrels).

• Morphological Adaptations for Gliding:

  • Patagium: The most obvious adaptation is the gliding membrane, or patagium.
  • Special Cartilages: Some species possess special cartilages that extend the patagium. For example, some large squirrels have an extra cartilage extending from the hand to expand the patagium.
  • Flattened Tail: A flattened tail is often observed, used for maneuvering during the glide.

• Hypotheses for the Evolution of Gliding (Not Mutually Exclusive):

  • Response to Habitat: Gliding is prevalent in specific forest types, such as those in Southeast Asia, characterized by very tall canopies and ample free space. This structure allows gliders to move between stratified layers of the forest.
  • Predator Avoidance:
    • Gliding offers more escape paths in three dimensions compared to two dimensions.
    • It allows gliders to stay off the ground, where many predators (like tigers) reside. Calugos, for instance, were observed to land on the ground only $4$ times out of $267$ glides.
    • Living arboreally is associated with increased longevity in mammals; arboreal taxa generally live longer for a given body size compared to terrestrial taxa (supported by data showing arboreal mammals having higher lifespan values on a body size vs. lifespan plot).
  • Energetic Efficiency: The hypothesis suggests gliding might be more energetically efficient than quadrupedal locomotion for covering the same distance.
    • Counter-evidence: Studies in Calugos suggest that while gliding saves time, it does not save energy. The energy required to climb vertically and then glide ($E<em>{climb}$) is higher than the energy for horizontal movement ($E</em>{horizontal}$) over the same distance. However, the total energy consumed by gliding is a very small percentage of the daily energy budget, so its energetic cost might not be a significant selective pressure.
  • Avoiding Injuries: Leaping between trees can lead to hard landings and injuries. Gliding allows for softer landings.
    • Evidence: For ballistic leapers (e.g., monkeys), landing impulse increases with the distance traveled, implying harsher landings over longer distances. For gliders, the landing impulse remains flat and constant regardless of glide distance because they maneuver their body and extend their patagium to land softly.
  • Specialized Diets: Many gliders consume specialized diets (gums, nectars, young leaves) which are often scattered and/or nutrient-poor. Gliding provides an efficient way to travel across space to find these dispersed food resources.
    • Evidence: Comparative analyses show a significant association between gliding evolution and the evolution of these specialized diets, indicating that foraging ecology influences locomotion.

• Phylogenetic Placement of Colugos (Flying Lemurs):

  • Early hypotheses were uncertain about their placement, but full genome sequencing now places Calugos as sister to primates.
  • They form part of the Euarchonta clade, which includes tree shrews (Scandentia), colugos (Dermoptera), and primates.
  • Along with rodents and rabbits (Glires), these form the superorder Euarchontoglires.
  • Shared Trait: Colugos, tree shrews, and early-diverging primates (strepsirrhines like lemurs) all possess a tooth comb. However, this is an example of convergent evolution, as the tooth comb morphology is not identical in detail across these groups.
  • Understanding Calugos is important for insights into primate origins and the transition toward the primate lineage.

Locomotion: Flying (Bats)

• Bats (Order Chiroptera): Flying did not evolve from gliding.
• Wing Morphology:
  • Elongated Digits: Bats possess greatly elongated metacarpals and phalanges, particularly digits $3$ through $5$ of the hand.
  • Patagium Components: The wing membrane (patagium) has multiple parts, including the propatagium (leading edge) and the chiropatagium (the hand wing).
• Evolutionary Puzzles:
  • Fossil Record: The relative lengths of bat digits have remained constant since the earliest known fossil bats (e.g., Icaronycteris). Living bats and fossil bats exhibit a consistent relationship between body size and the length of the fifth metacarpal, all falling on the same line. This suggests a potentially rapid and distinctive morphological evolution without clear "missing links," contrasting with fossil records of other groups like whales.
• Developmental Evolution of Bat Wings:
  • Embryonic Development: At certain developmental stages (e.g., stage $16$), an embryonic bat's hand looks similar to that of a typical mammal (e.g., a mouse).
  • Late Elongation: A profound and rapid elongation of the fingers, particularly the fifth metacarpus, occurs late in bat development.
  • Genetic Basis: Research identified relatively few genes responsible for this rapid digit elongation. Specifically, the protein BMP2 (Bone Morphogenetic Protein 2) was found to be upregulated, meaning its expression levels are increased, driving the elongation of the bat forelimb elements.
• Genotype-Phenotype Relationships: Structural vs. Regulatory Change:
  • This bat example illustrates regulatory change in evolution:
    • The proteins themselves (their amino acid sequences) may not have evolved significantly. Instead, the regulation of their expression during development has changed (e.g., increased BMP2 expression).
  • This contrasts with structural change (e.g., protein evolution via amino acid substitutions), as seen in beach mice's light coloration. Both structural and regulatory changes can lead to rapid phenotypic evolution.

Bat Wing Evolution and Ecology: Eco-morphology

• Ecological Diversity of Bats: Bats are incredibly diverse ecologically, with specialized wings reflecting their ecological roles.
• Key Wing Shape Parameters:
  • Wing Loading (WL):
    • Definition: Ratio of weight to wing area (WL = rac{ ext{Weight}}{ ext{Wing Area}}).
    • Low loading: Characterizes bats with small, light bodies and/or relatively large wing surface areas (high wing per unit body mass). This allows them to fly slowly and generate lift easily, enabling easy take-off even from the ground.
  • Aspect Ratio (AR):
    • Definition: Ratio of the square of the wingspan to the wing area (AR = rac{ ext{Wingspan}^2}{ ext{Wing Area}}). This is a measure of wing shape.
    • High aspect ratio: Indicates long, skinny wings, optimal for sustained, rapid flight (similar to swifts or swallows in birds).
• Eco-morphological Correlations: Bat wing shapes are strongly correlated with their foraging ecology:
  • High Loading, High Aspect Ratio (Long, Skinny Wings):
    • Example: Free-tailed bats (e.g., Tadarida brasiliensis).
    • Adaptation: Suited for fast, efficient flight in open spaces, often at high altitudes and for extended periods throughout the night (like "race cars").
    • Roosting Implications: Due to high wing loading, they cannot easily take off from low positions. They typically roost high (e.g., under bridges, on cliffs, in high caves) and drop to gain airspeed before flight.
  • Low Loading, Low Aspect Ratio (Short, Broad Wings):
    • Examples: Hover-gleaners (glean insects from vegetation/tree trunks), ground gleaners (e.g., pallid bats, Antrozous pallidus which eat scorpions).
    • Adaptation: Ideal for slow, highly maneuverable flight in cluttered habitats (e.g., dense forests, close to the ground).
    • Foraging and Roosting: Can land, move on the ground (e.g., to catch scorpions), and easily take off again due to their low wing loading. Some may even roost in rodent burrows on the ground.
  • Specialized Carnivores (Non-Fish Eaters) and Piscivores (Fish Eaters):
    • These bats (e.g., Trachops eating frogs) often exhibit eco-morphological convergence, evolving similar low loading, low aspect ratio wing shapes independently, as these wing designs facilitate their specific foraging strategies (e.g., gleaning prey from surfaces or water).
    • This demonstrates how distinct lineages can evolve similar morphological solutions to similar ecological challenges.