Person:

Moore, Talia Yuki

Bipedalism is commonly assumed to be an adaptive convergence because it has evolved independently three times in small desert rodents. However, the functional benefits of bipedality in this ecosystem have long been unclear. In this thesis I integrate phylogenetics, functional morphology, biomechanics, information theory, and behavior to investigate whether and how bipedality increases fitness in desert ecosystems, and whether bipedal rodents convergently evolved to have the role in their respective ecosystems.

Based on the diversity of extant dipodid rodents, I begin by statistically reconstructing the pattern of morphological evolution in jerboas. I find that the strongest indicator of bipedality is metatarsal to humerus length, and that changes in this ratio are associated with increased rates of speciation, supporting a punctuated equilibrium pattern of evolution in this clade. Furthermore, the distinct patterns of morphological evolution suggest that a complex suite of genetic and developmental mechanisms governs the acquisition of bipedality in jerboas.

I then use an inverse dynamics approach to characterize the biomechanics of bipedal hopping in a derived jerboa. I find that the dynamics of jerboa hopping are generated predominantly by muscular contractions, rather than tendon--based elastic energy storage and return between strides. Therefore hopping in small rodents favors rapid production and absorption of forces, rather than sustained bouts of steady--state locomotion.

By reviewing predator--prey studies in biomechanics, ecology, and evolution I hypothesize that ricochetal locomotion enhances the ability of small rodents to evade predators that hunt via ballistic interception. I then develop Information Theoretic techniques to measure the unpredictability of escape trajectories in sympatric bipedal and quadrupedal rodents. As expected, bipedal rodents use significantly more unpredictable escape trajectories, likely enhancing predator evasion ability and enabling foraging in exposed areas with higher predation risk. I then found that bipedal rodents exhibit a stronger preference for exploring open spaces, matching previously established foraging patterns. These findings suggest that the evolution of bipedality enables spatial resource partitioning to limit interspecific competition in desert rodents.

Based on the functional studies in my thesis, I evaluate ecological models to predict the occurrence of convergent bipedal rodents in Myomorpha. I show that diet specialization and aridity are insufficient to predict the locomotor morphology of these rodents and develop novel hypotheses for the convergent evolution of bipedalism in desert rodents.

My thesis investigates the functional consequences of morphological evolution in the context of evolutionary ecology. By considering the interconnectedness of ecology, behavior, and evolution, studies in biomechanics can be designed to inform each of these fields. This interdisciplinary approach is necessary to study the adaptive nature of behavioral traits that are governed by myriad genetic, developmental, and environmental factors.

Mechanistically linking movement behaviors and ecology is key to understanding the adaptive evolution of locomotion. Predator evasion, a behavior that enhances fitness, may depend upon short bursts or complex patterns of locomotion. However, such movements are poorly characterized by existing biomechanical metrics. We present methods based on the entropy measure of randomness from Information Theory to quantitatively characterize the unpredictability of non-steady-state locomotion. We then apply the method by examining sympatric rodent species whose escape trajectories differ in dimensionality. Unlike the speed regulated gait use of cursorial animals to enhance locomotor economy, bipedal jerboa (family Dipodidae) gait transitions likely enhance maneuverability. In field-based observations, jerboa trajectories are significantly less predictable than those of quadrupedal rodents, likely increasing predator evasion ability. Consistent with this hypothesis, jerboas exhibit lower anxiety in open fields than quadrupedal rodents, a behavior that varies inversely with predator evasion ability. Our unpredictability metric expands the scope of quantitative biomechanical studies to include non-steady-state locomotion in a variety of evolutionary and ecologically significant contexts.

Behavioral studies performed in natural habitats provide a context for the development of hypotheses and the design of experiments relevant both to biomechanics and to evolution. In particular, predator–prey interactions are a model system for integrative study because success or failure of predation has a direct effect on fitness and drives the evolution of specialized performance in both predator and prey. Although all predators share the goal of capturing prey, and all prey share the goal of survival, the behavior of predators and prey are diverse in nature. This article presents studies of some predator–prey interactions sharing common predation strategies that reveal general principles governing the behaviors of predator and prey, even in distantly related taxa. Studies of predator–prey interactions also reveal that maximal performance observed in a laboratory setting is not necessarily the performance that determines fitness. Thus, considering locomotion in the context of predation ecology can aid in evolutionarily relevant experimental design. Classification by strategy reveals that displaying unpredictable trajectories is a relevant anti-predator behavior in response to multiple predation strategies. A predator’s perception and pursuit of prey can be affected indirectly by divergent locomotion of similar animals that share an ecosystem. Variation in speed and direction of locomotion that directly increases the unpredictability of a prey’s trajectory can be increased through genetic mutation that affects locomotor patterns, musculoskeletal changes that affect maneuverability, and physical interactions between an animal and the environment. By considering the interconnectedness of ecology, physical constraints, and the evolutionary history of behavior, studies in biomechanics can be designed to inform each of these fields.

Recent rapid advances in experimental biology have expanded the opportunity for interdisciplinary investigations of the evolution of form and function in non-traditional model species. However, historical divisions of philosophy and methodology between evolutionary/organismal biologists and developmental geneticists often preclude an effective merging of disciplines. In an effort to overcome these divisions, we take advantage of the extraordinary morphological diversity of the rodent superfamily Dipodoidea, including the bipedal jerboas, to experimentally study the developmental mechanisms and biomechanical performance of a remarkably divergent limb structure. Here, we place multiple limb character states in a locomotor and phylogenetic context. Whereas obligate bipedalism arose just once in the ancestor of extant jerboas, we find that digit loss, metatarsal fusion, between-limb proportions, and within-hindlimb proportions all evolved independently of one another. Digit loss occurred three times through at least two distinct developmental mechanisms, and elongation of the hindlimb relative to the forelimb is not simply due to growth mechanisms that change proportions within the hindlimb. Furthermore, we find strong evidence for punctuated evolution of allometric scaling of hindlimb elements during the radiation of Dipodoidea. Our work demonstrates the value of leveraging the evolutionary history of a clade to establish criteria for identifying the developmental genetic mechanisms of morphological diversification.