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ABSTRACT Much of our understanding of human physiological responses to exercise comes from human or rodent exercise models. In particular, there is clear evidence that endurance-trained individuals have increased fat breakdown, but only after weeks of physical training. In contrast, long-distance migratory animals such as birds, fish and insects exhibit increased activity of the molecular machinery involved in fat breakdown even before the exercise stressor occurs. Additionally, these migratory species rely more on fatty acids to meet the 85% VO2,max energy demand of flight compared with humans exercising at the same workload. This underscores the superior ability of migratory animals to use the energy-rich fuel of fatty acids. Despite long-distance migration being studied for decades, only a few studies have directly compared one or two ultra-athletic taxa. This Review examines diet selection, mobilization and transport, uptake and breakdown, and mitochondrial respiratory capacity in humans, migratory birds, fish and insects. Our goal is to provide a comprehensive comparison of these taxa, highlighting the degree to which the molecular machinery involved in fat breakdown is conserved, despite differences in fuel selection and preferences that enable them to meet the energy demands of long-distance exercise. 

Abstract Aerobic respiration in mitochondria is the source for most of the energy that powers complex animals, and maintaining energy flow from mitochondria near the optimum needed for life processes presents challenges for complex animals. Environments of most animals change rapidly. Moreover, individuals pass through developmental stages with different energy demands, and they shift life-history states that require modified production of adenosine triphosphate (ATP). To adjust to changing conditions, all complex animals display some capacity for acclimatization through phenotypic flexibility, whereby key aspects of mitochondrial respiration are reversibly altered. Phenotypic flexibility is a universal feature of the energy-production mechanisms of animals, but all animals face limitations in the range of environments and circumstances to which they can acclimatize. We discuss multiple examples of such phenotypic flexibility in animals, focusing on the different mechanisms employed that acclimatize mitochondrial respiration to exogenous and endogenous challenges. Genotype sets the range of phenotypes related to mitochondrial respiration that is available to an animal. Numerous studies document adaptive evolution of both mitochondrial and nuclear genes that directly affect the range of environments that will support oxidative phosphorylation. Phenotypic flexibility can obscure evolutionary changes in response to changing energy demands, and understanding the interplay of capacity for acclimatization and adaptive evolution of mitochondrial systems presents major challenges for physiological and evolutionary biologists. 

Synopsis Avian migration is among the most energetically demanding feats observed in animals. Studies evaluating the physiological underpinnings of migration have repeatedly shown that migratory birds display numerous adaptations that ultimately supply the flight muscle mitochondria with abundant fuel and oxygen during long-distance flights. To make use of this high input, the organs and mitochondria of migrants are predicted to display several traits that maximize their capacity to produce adenosine triphosphate (ATP). This review aims to introduce readers to several mechanisms by which organs and mitochondria can alter their capacity for oxidative phosphorylation and ATP production. The role of organ size, mitochondrial volume, substrate, and oxygen delivery to the electron transport system are discussed. A central theme of this review is the role of changes in electron chain complex activity, mitochondrial morphology and dynamics, and supercomplexes in allowing avian migrants and other taxa to alter the performance of the electron transport system with predictable shifts in demand. It is my hope that this review will serve as a springboard for future studies exploring the mechanisms that alter bioenergetic capacity across animal species. 

Synopsis The cost of supporting traits that increase mating opportunities and maximize the production of quality offspring is paid in energy. This currency of reproduction is enabled by bioenergetic adaptations that underlie the flexible changes in energy utilization that occur with reproduction. This review considers the traits that contribute to variation in the capacity of an organ to produce ATP. Further, it synthesizes findings from studies that have evaluated bioenergetic adaptations to the production of sexually selected traits and performance during reproduction and the role of change in mitochondrial respiratory performance in the tradeoff between reproduction and longevity. Cumulatively, these works provide evidence that in selecting for redder males, female finches will likely mate with a male with high mitochondrial respiratory performance and, potentially, a higher probability of mitonuclear compatibility. Females from diverse taxa allocate more to reproduction when the respiratory performance of mitochondria or density of the inner mitochondrial membrane in the liver or skeletal muscle is higher. Finally, reproduction does not appear to have persistent negative effects on mitochondrial respiratory performance, countering a role for mitochondria in the trade-off between reproduction and longevity. I close by noting that adaptations that improve mitochondrial respiratory performance appear vital for optimizing reproductive fitness. 

Synopsis Birds exhibit a variety of migration strategies. Because sustained flapping flight requires the production of elevated levels of energy compared to typical daily activities, migratory birds are well-documented to have several physiological adaptations to support the energy demands of migration. However, even though mitochondria are the source of ATP that powers flight, the respiratory performance of the mitochondria is almost unstudied in the context of migration. We hypothesized that migratory species would have higher mitochondrial respiratory performance during migration compared to species that do not migrate. To test this hypothesis, we compared variables related to mitochondrial respiratory function between two confamilial bird species—the migratory Gray Catbird (Dumetella carolinensis) and the non-migratory Northern Mockingbird (Mimus polyglottos). Birds were captured at the same location along the Alabama Gulf Coast, where we assumed that Gray Catbirds were migrants and where resident Northern Mockingbirds live year-round. We found a trend in citrate synthase activity, which suggests that Gray Catbirds have a greater mitochondrial volume in their pectoralis muscle, but we observed no other differences in mitochondrial respiration or complex enzymatic activities between individuals from the migrant vs. the non-migrant species. However, when we assessed the catbirds included in our study using well-established indicators of migratory physiology, birds fell into two groups: a group with physiological parameters indicating a physiology of birds engaged in migration and a group with the physiology of birds not migrating. Thus, our comparison included catbirds that appeared to be outside of migratory condition. When we compared the mitochondrial performance of these three groups, we found that the mitochondrial respiratory capacity of migrating catbirds was very similar to that of Northern Mockingbirds, while the catbirds judged to be not migrating were lowest. One explanation for these observations is these species display very different daily flight behaviors. While the mockingbirds we sampled were not breeding nor migrating, they are highly active birds, living in the open and engaging in flapping flights throughout each day. In contrast, Gray Catbirds live in shrubs and fly infrequently when not migrating. Such differences in baseline energy needs likely confounded our attempt to study adaptations to migration. 

The migratory movements undertaken by birds are among the most energetically demanding behaviours observed in nature. Mitochondria are the source of aerobic energy production on which migration depends, but a key component of mitochondrial function, mitochondrial remodelling, has not been investigated in the context of bird migration. We measured markers of mitochondrial remodelling in the skeletal muscles of the Gambel’s (migratory) and Nuttall’s (non-migratory) white-crowned sparrows within and outside migratory periods. Gambel’s were collected in (i) a non-migration period (baseline), (ii) preparation to depart for spring migration (pre-migration) and (iii) active autumn migration (mid-migration). Nuttall’s were collected at timepoints corresponding to baseline and mid-migration in Gambel’s. Across all sampling periods, we found that migratory birds had greater mitochondrial remodelling compared with non-migratory birds. Furthermore, birds from the migratory population also displayed flexibility, increasing several markers of mitochondrial remodelling (e.g. NRF1, OPA1 and Drp1) pre- and during migration. Further, the greater levels of mitochondrial remodelling and its upregulation during migration were specific to the pectoralis muscle used in flapping flight. Our study is the first to show that mitochondrial remodelling supports migration in Gambel’s white-crowned sparrows, indicating a highly specific and efficient phenotype supporting the increased energetic demands of migration. 

Abstract Migration is one of the most energy-demanding behaviors observed in birds. Mitochondria are the primary source of energy used to support these long-distance movements, yet how mitochondria meet the energetic demands of migration is scarcely studied. We quantified changes in mitochondrial respiratory performance in the White-crowned Sparrow (Zonotrichia leucophrys), which has a migratory and non-migratory subspecies. We hypothesized that the long-distance migratory Gambel’s subspecies (Z. l. gambelii) would show higher mitochondrial respiratory performance compared to the non-migratory Nuttall’s subspecies (Z. l. nuttalli). We sampled Gambel’s individuals during spring pre-migration, active fall migration, and a period with no migration or breeding (winter). We sampled Nuttall’s individuals during periods coinciding with fall migration and the winter period of Gambel’s annual cycle. Overall, Gambel’s individuals had higher citrate synthase, a proxy for mitochondrial volume, than Nuttall’s individuals. This was most pronounced prior to and during migration. We found that both OXPHOS capacity (state 3) and basal respiration (state 4) of mitochondria exhibit high seasonal flexibility within Gambel’s individuals, with values highest during active migration. These values in Nuttall’s individuals were most similar to Gambel’s individuals in winter. Our observations indicate that seasonal changes in mitochondrial respiration play a vital role in migration energetics. 

Abstract Trade-offs resulting from the high demand of offspring production are a central focus of many subdisciplines within the field of biology. Yet, despite the historical and current interest on this topic, large gaps in our understanding of whole-organism trade-offs that occur in reproducing individuals remain, particularly as it relates to the nuances associated with female reproduction. This volume of Integrative and Comparative Biology (ICB) contains a series of papers that focus on reviewing trade-offs from the female-centered perspective of biology (i.e., a perspective that places female reproductive biology at the center of the topic being investigated or discussed). These papers represent some of the work showcased during our symposium held at the 2024 meeting of the Society for Integrative and Comparative Biology (SICB) in Seattle, Washington. In this roundtable discussion, we use a question-and-answer format to capture the diverse perspectives and voices involved in our symposium. We hope that the dialogue featured in this discussion will be used to motivate researchers interested in understanding trade-offs in reproducing females and provide guidance on future research endeavors.