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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 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. 

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. 

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. 

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.