Flight Muscle Development Research Articles

Bruno 1/CELF regulates splicing and cytoskeleton dynamics to ensure correct sarcomere assembly in Drosophila flight muscles.

Muscles undergo developmental transitions in gene expression and alternative splicing that are necessary to refine sarcomere structure and contractility. CUG-BP and ETR-3-like (CELF) family RNA-binding proteins are important regulators of RNA processing during myogenesis that are misregulated in diseases such as Myotonic Dystrophy Type I (DM1). Here, we report a conserved function for Bruno 1 (Bru1, Arrest), a CELF1/2 family homolog in Drosophila, during early muscle myogenesis. Loss of Bru1 in flight muscles results in disorganization of the actin cytoskeleton leading to aberrant myofiber compaction and defects in pre-myofibril formation. Temporally restricted rescue and RNAi knockdown demonstrate that early cytoskeletal defects interfere with subsequent steps in sarcomere growth and maturation. Early defects are distinct from a later requirement for bru1 to regulate sarcomere assembly dynamics during myofiber maturation. We identify an imbalance in growth in sarcomere length and width during later stages of development as the mechanism driving abnormal radial growth, myofibril fusion, and the formation of hollow myofibrils in bru1 mutant muscle. Molecularly, we characterize a genome-wide transition from immature to mature sarcomere gene isoform expression in flight muscle development that is blocked in bru1 mutants. We further demonstrate that temporally restricted Bru1 rescue can partially alleviate hypercontraction in late pupal and adult stages, but it cannot restore myofiber function or correct structural deficits. Our results reveal the conserved nature of CELF function in regulating cytoskeletal dynamics in muscle development and demonstrate that defective RNA processing due to misexpression of CELF proteins causes wide-reaching structural defects and progressive malfunction of affected muscles that cannot be rescued by late-stage gene replacement.

Evolution, types, and distribution of flight control devices on wings and elytra in bark beetles

Gaining the ability to fly actively was a ground-breaking moment in insect evolution, providing an unprecedented advantage over other arthropods. Nevertheless, active flight was a costly innovation, requiring the development of wings and flight muscles, the provision of sufficient energetic resources, and a complex flight control system. Although wings, flight muscles, and the energetic budget of insects have been intensively studied in the last decades, almost nothing is known regarding the flight-control devices of many crucial insect groups, especially beetles (Coleoptera). Here, we conducted a phylogenetic-informed analysis of flight-related mechanosensors in 28 species of bark beetles (Curculionidae: Scolytinae, Platypodinae), an economically and ecologically important group of insects characterized by striking differences in dispersal abilities. The results indicated that beetle flight apparatus is equipped with different functional types of mechanosensors, including strain- and flow-encoding sensilla. We found a strong effect of allometry on the number of mechanosensors, while no effect of relative wing size (a proxy of flight investment) was identified. Our study constitutes the first step to understanding the drivers and constraints of the evolution of flight-control devices in Coleoptera, including bark beetles. More research, including a quantitative neuroanatomical analysis of beetle wings, should be conducted in the future.

Distinct developmental patterns in Anopheles stephensi organ systems

Anatomical profiles of insects inform vector biology, comparative development and evolutionary studies with applications in forensics, agriculture and disease control. This study presents a comprehensive, high-resolution developmental profile of Anopheles stephensi, encompassing larval, pupal, and adult stages, obtained through microCT scanning. The results indicate in situ anatomical changes in most organ systems, including the central nervous system, eyes, musculature, alimentary canal, salivary glands, and ovaries, among other organ systems, except for the developing heart. We find significant differences in the mosquito gut, body-wall, and flight muscle development during metamorphosis from other dipterans like Drosophila. Specifically, indirect flight muscle specification and growth can be traced back at least to the 4th instar A. stephensi larvae, as opposed to post-puparial development in other Dipterans like Drosophila and Calliphora. Further, while Drosophila larval body-wall muscles and gut undergo histolysis, changes to these organs during mosquito metamorphosis are less pronounced. These observations, and raw data therein may serve as a reference for studies on the development and the genetics of mosquitoes. Overall, the detailed developmental profile of A. stephensi presented here illuminates the unique anatomy and developmental processes of Culicidae, with important implications for vector biology, disease control, and comparative evolutionary studies.

Relationship between flight muscle dimorphism and wing morphometry in Triatoma infestans (Klug, 1834) (Hemiptera, Reduviidae, Triatominae)

Triatoma infestans, the primary vector of Chagas disease in southern South America, is reported as a dimorphic species for flight muscle development and presents a marked phenotypic plasticity in traits related to flight. In triatomines, studying the relationship between flight muscle development and wing variation is important, since it involves flight capacity and dispersion. Therefore, we examined the association between flight muscle dimorphism and morphological wing variation in T. infestans individuals. We hypothesized that if the underdeveloped flight muscle were associated with a decrease in wing developmental stability, canalization and morphological aspect of wings, and with a loss of wing modularity, then wing variation would be associated with flight muscle dimorphism. Wing size and shape were characterized using geometric morphometrics. Patterns of canalization, developmental instability, and modularity were inferred from fluctuating asymmetry analysis of wing shape. Morphological aspects of wings were estimated using maximum wing length and wing area. The results showed that there are differences in wing shape but not in wing size among groups. Canalization and developmental stability were positively associated in individuals with muscle development and negatively associated in individuals with underdeveloped flight muscles. The covariance structure of variation among individuals was different between groups but not for fluctuating asymmetry, both for females and males. Modularity hypothesis related to the wing subdivision into two parts, a stiff part and a membranous one, showed significant association for the variation among individuals and fluctuating asymmetry variation in females with flight muscles. Wing aspect showed that females with flight muscles exhibited more elongated and thinner wings than those without flight muscles. The results obtained in this study reveal an association between flight muscle development and forewing variation in T. infestans. Females with flight muscles have certain differential characteristics in their wings that would be related to an enhanced flight performance.

Larval diet impacts flight performance in monarch butterflies

Abstract Few studies have described the effects of larval diet quality on adult insect flight performance. Flight muscle development and high‐powered flight in insects are associated with costly energetic demands. Because larval diet is the energy source that powers these mechanisms, we asked whether larval diet has an impact on flight performance and metabolism in the monarch butterfly (Danaus plexippus Linnaeus). Monarch caterpillars from the eastern North American and Puerto Rican populations were fed a diet of either Asclepias incarnata L. (native to the eastern North American population) or Asclepias curassavica L. (native to the Puerto Rican population and uncommon in eastern North America). We flew the monarchs on a tethered flight mill to acquire flight performance metrics including velocity, distance, duration, power, and oxygen consumption rate. Monarchs reared on the A. incarnata L. milkweed showed slower, shorter, and less powerful flights than those fed on A. curassavica L. However, eastern North American and Puerto Rican monarchs, which were reared under summer conditions, did not differ in flight metrics or post‐flight metabolic rates. The results suggest that flight in eastern North American and Puerto Rican monarchs is similar during the breeding season, yet the milkweed the caterpillars consume has important implications for flight performance.

M1BP is an essential transcriptional activator of oxidative metabolism during Drosophila development

Oxidative metabolism is the predominant energy source for aerobic muscle contraction in adult animals. How the cellular and molecular components that support aerobic muscle physiology are put in place during development through their transcriptional regulation is not well understood. Using the Drosophila flight muscle model, we show that the formation of mitochondria cristae harbouring the respiratory chain is concomitant with a large-scale transcriptional upregulation of genes linked with oxidative phosphorylation (OXPHOS) during specific stages of flight muscle development. We further demonstrate using high-resolution imaging, transcriptomic and biochemical analyses that Motif-1-binding protein (M1BP) transcriptionally regulates the expression of genes encoding critical components for OXPHOS complex assembly and integrity. In the absence of M1BP function, the quantity of assembled mitochondrial respiratory complexes is reduced and OXPHOS proteins aggregate in the mitochondrial matrix, triggering a strong protein quality control response. This results in isolation of the aggregate from the rest of the matrix by multiple layers of the inner mitochondrial membrane, representing a previously undocumented mitochondrial stress response mechanism. Together, this study provides mechanistic insight into the transcriptional regulation of oxidative metabolism during Drosophila development and identifies M1BP as a critical player in this process.

Developmental origin of tendon diversity in Drosophila melanogaster.

Myogenesis is a developmental process that is largely conserved in both Drosophila and higher organisms. Consequently, the fruit fly is an excellent in vivo model for identifying the genes and mechanisms involved in muscle development. Moreover, there is growing evidence indicating that specific conserved genes and signaling pathways govern the formation of tissues that connect the muscles to the skeleton. In this review, we present an overview of the different stages of tendon development, from the specification of tendon progenitors to the assembly of a stable myotendinous junction across three different myogenic contexts in Drosophila: larval, flight and leg muscle development. We underline the different aspects of tendon cell specification and differentiation in embryo and during metamorphosis that result into tendon morphological and functional diversity.

Energy Utilization and Flight Muscle Development in Chrysoperla sinica (Neuroptera: Chrysopidae) Female Adults: Relationship With Age and Flight Behavior.

We investigated the accumulation of energy substances, dynamics of flight muscle development, changes in energy substances accumulation, and flight muscle structure after flight activities in female adults of the green lacewing Chrysoperla sinica (Tjeder), a common natural enemy of various insect pests in China. Virgin individuals were chosen at 24, 72, and 120 h after eclosion for energy substance determination and flight muscle observation in this study. Individuals with strong flight ability at 72 h after eclosion were selected for tethered flight assays, followed by detection of energy substances, and flight muscle observation. The results showed that virgin female adults had the highest fat content 72 h after eclosion. Sarcomere length and myofibril diameter changed significantly with age, with the lowest at 24 h after eclosion. With an increase in flight distance, the fat and glycogen contents, sarcomere length, and volume fraction of the transverse tubular system (T-system) decreased and myofibril diameters increased. The volume fraction of the mitochondria did not significantly change, but the structure of the mitochondrial membrane was destroyed, inclusions were reduced, and cavities appeared. The reserves of energy substances, especially lipids, are closely related to the flight ability of C. sinica. The observational results of both flight muscle structure and morphology of mitochondria build a strong relationship with flight behavior. This research should help reveal the regulatory mechanism of flight activity of C. sinica.

Myoblast proliferation during flight muscle development in Manduca sexta is unaffected by reduced neural signaling

In holometabolous insects, metamorphosis involves restructuring the musculature to accommodate adult-specific anatomy and behaviors. Evidence from experiments on remodeled muscles, as well as those that develop de novo, suggests that signals from the nervous system support adult muscle development by controlling myoblast proliferation rate. However, the dorsolongitudinal flight muscles (DLMs) of Manduca sexta undergo a mixed developmental program involving larval muscle fibers, and it is not known if neurons play the same role in the formation of these muscles. To address this question, we have blocked the most promising candidate pathways for neural input and examined the DLMs for changes in proliferation. Our results show that DLM development does not depend on neural activity, Hedgehog signaling, or EGF signaling. It remains to be determined how DLM growth is controlled and why neurally mediated proliferation differs between individual muscles.

Reproduction does not impede the stopover departure to ensure a potent migration in Cnaphalocrocis medinalis moths.

Despite the importance of reproduction in insects, its relation with multi-stop flight remains poorly understood in migratory species. To clarify whether reproductive maturation commences during the multi-stop flight or after the completion of migration, we conducted physiological and behavioral assays in the rice leaf roller Cnaphalocrocis medinalis with laboratory-simulated conditions and field-captured populations. We found that the ovarian development was significantly promoted by tethered flight treatment for 1-2 nights when compared to the unflown group, while the flight muscle development was not impaired. There was no significant difference in flight duration, flight distance and flight velocity between mated and virgin female moths, indicating that mated moths remained competent for the subsequent flights as did the virgins. Using an integrated field assay, we identified that over 60% of the female moths in the migrating populations captured by high-altitude searchlights in the Immigration period of a season had completed the ovarian development and mating. Sexually mature and mated moths collected in the rice field in the Emigration period were found capable of engaging in migratory take-off, as observed using an indoor monitoring platform. Overall, our findings point out that C. medinalis managed to complete reproductive maturation to a large extent during the multi-stop migratory flight without compromising the migration performance. Such a cost-effective strategy ensures a successful migration for the moths. These findings advance our understanding of the relationship between reproduction and migration, thus shedding light on the development of novel control measures for the outbreak of migratory insect pests.

Myoblast Proliferation During Flight Muscle Development in Manduca Sexta is Unaffected by Reduced Neural Signaling

Myoblast Proliferation During Flight Muscle Development in Manduca Sexta is Unaffected by Reduced Neural Signaling

Development of the indirect flight muscles of Aedes aegypti, a main arbovirus vector

BackgroundFlying is an essential function for mosquitoes, required for mating and, in the case of females, to get a blood meal and consequently function as a vector. Flight depends on the action of the indirect flight muscles (IFMs), which power the wings beat. No description of the development of IFMs in mosquitoes, including Aedes aegypti, is available.MethodsA. aegypti thoraces of larvae 3 and larvae 4 (L3 and L4) instars were analyzed using histochemistry and bright field microscopy. IFM primordia from L3 and L4 and IFMs from pupal and adult stages were dissected and processed to detect F-actin labelling with phalloidin-rhodamine or TRITC, or to immunodetection of myosin and tubulin using specific antibodies, these samples were analyzed by confocal microscopy. Other samples were studied using transmission electron microscopy.ResultsAt L3–L4, IFM primordia for dorsal-longitudinal muscles (DLM) and dorsal–ventral muscles (DVM) were identified in the expected locations in the thoracic region: three primordia per hemithorax corresponding to DLM with anterior to posterior orientation were present. Other three primordia per hemithorax, corresponding to DVM, had lateral position and dorsal to ventral orientation. During L3 to L4 myoblast fusion led to syncytial myotubes formation, followed by myotendon junctions (MTJ) creation, myofibrils assembly and sarcomere maturation. The formation of Z-discs and M-line during sarcomere maturation was observed in pupal stage and, the structure reached in teneral insects a classical myosin thick, and actin thin filaments arranged in a hexagonal lattice structure.ConclusionsA general description of A. aegypti IFM development is presented, from the myoblast fusion at L3 to form myotubes, to sarcomere maturation at adult stage. Several differences during IFM development were observed between A. aegypti (Nematoceran) and Drosophila melanogaster (Brachyceran) and, similitudes with Chironomus sp. were observed as this insect is a Nematoceran, which is taxonomically closer to A. aegypti and share the same number of larval stages.

Dispersal–reproduction trade‐off in the leaf beetleGalerucella grisescens

AbstractDispersion–reproduction trade‐offs are important to explore the evolutionary mechanism of dispersal strategies and the adaptive significance of dispersion in insects. In our previous study, variations in hindwing length were found in Japanese populations of the leaf beetleGalerucella grisescens(Joannis) (Coleoptera: Chrysomelidae). They were distinctly divided into either long‐winged (LW) or short‐winged (SW) morphs in the field. The LW morphs were distributed widely in Japan, whereas the SW morphs were found in restricted areas in Honshu, the main island of Japan. We examined the possible existence of trade‐offs between dispersion and reproduction inG.grisescensby laboratory experiments. Larval duration and adult body size (head width) were not significantly different between LW and SW strains, but adult body weight was larger in some LW strains than in SW strains, most likely due to the size of hindwings and legs as well as to the development of flight muscles. Although the pre‐oviposition period was not significantly different among strains, female longevity and fertility were significantly higher in SW than in LW strains. Long‐winged individuals displayed flutter behaviours, suggesting their flight dispersal abilities, but SW individuals did not. Femurs of LW individuals were significantly longer on all legs compared to SW strains and the former walked faster than the latter. The present results indicate the presence of a dispersion–reproduction trade‐off inG. grisescens, in which SW strains have advantages in reproductive abilities and LW strains in dispersal abilities.

Starvation on First or Second Day of Adulthood Reverses Larval-Stage Decision to Migrate in Beet Webworm (Lepidoptera: Pyralidae).

A facultative commitment to adult migration in the larval stage can be modified again after adult emergence in some Lepidoptera when influenced by an appropriate environmental cue during a sensitive stage. This phenomenon is termed secondary regulation of migration. The sensitive stage in adult beet webworm, Loxostege sticticalis L. (Lepidoptera: Pyralidae), was determined experimentally by starvation of presumed migrant females reared from gregarious-phase larvae (induced by crowding at 10 larvae per 650-ml jar). When presumed migrant adults were starved for 24 h on either of the first 2 d after emergence, the preoviposition period was shortened. In contrast, preoviposition periods were not significantly shortened for migrants starved on day 3 or when starvation lasted for more than 1 d after emergence. Because the preoviposition period corresponds to the migratory period in beet webworm, the results suggest that the first 2 d of adult life in the beet webworm is the sensitive stage during which presumed migrants can be switched to residents by an appropriate environmental cue. During the sensitive stage or not, starvation did not influence lifetime fecundity, oviposition period, longevity, or hatching rate of eggs laid by the starvation-stressed moths. Starvation on the first day also increased tethered flight performance and accelerated both flight muscle and ovarian development. The results suggest that a pulse of starvation in the sensitive period may inhibit the expected migration by accelerating and compressing the cycle of migratory flight muscle development and degeneration, while accelerating ovarian development, which is normally suppressed until after migration.

Mechano-chemical enforcement of tendon apical ECM into nano-filaments during Drosophila flight muscle development

Contractile tension is critical for musculoskeletal system development and maintenance. In insects, the muscular force is transmitted to the exoskeleton through the tendon cells and tendon apical extracellular matrix (ECM). In Drosophila, we found tendon cells secrete Dumpy (Dpy), a zona pellucida domain (ZPD) protein, to form the force-resistant filaments in the exuvial space, anchoring the tendon cells to the pupal cuticle. We showed that Dpy undergoes filamentous conversion in response to the tension increment during indirect flight muscle development. We also found another ZPD protein Quasimodo (Qsm) protects the notum epidermis from collapsing under the muscle tension by enhancing the tensile strength of Dpy filaments. Qsm is co-transported with Dpy in the intracellular vesicles and diffuses into the exuvial space after secretion. Tissue-specific qsm expression rescued the qsm mutant phenotypes in distant tissues, suggesting Qsm can function in a long-range, non-cell-autonomous manner. In the cell culture assay, Qsm interacts with Dpy-ZPD and promotes secretion and polymerization of Dpy-ZPD. The roles of Qsm underlies the positive feedback mechanism of force-dependent organization of Dpy filaments, providing new insights into apical ECM remodeling through the unconventional interaction of ZPD proteins.

Marf-mediated mitochondrial fusion is imperative for the development and functioning of indirect flight muscles (IFMs) in drosophila

Dynamic changes in mitochondrial shape and size are vital for mitochondrial health and for tissue development and function. Adult Drosophila indirect flight muscles contain densely packed mitochondria. We show here that mitochondrial fusion is critical during early muscle development (in pupa) and that silencing of the outer mitochondrial membrane fusion gene, Marf, in muscles results in smaller mitochondria that are functionally defective. This leads to abnormal muscle development resulting in muscle dysfunction in adult flies. However, post-developmental silencing of Marf has no obvious effects on mitochondrial and muscle phenotype in adult flies, indicating the importance of mitochondrial fusion during early muscle development.

Inferring Cell Cycle Phases From a Partially Temporal Network of Protein Interactions

The temporal organisation of biological systems into phases and sub-phases is often crucial to their functioning. Identifying this multiscale organisation can yield insight into the underlying biological mechanisms at play. To date, however, this identification requires a priori biological knowledge of the system. Here, we put forward a new method to identify the temporal organisation of the cell cycle into phases and sub-phases, in an automated way. To do so, we model the cell cycle as a partially temporal network of protein-protein interactions (PPIs) by combining a traditional static PPI network with PPI time series data. Then, we cluster the snapshots of this temporal network to obtain phases. We first apply the method to the well known cell cycle of budding yeast, obtaining a good agreement with our biological knowledge of the cell cycle. We systematically test the robustness of the approach and investigate the effect of having only partial temporal information. In addition, we identify the phase arrests of cell cycle mutants, and infer mitochondrial state transitions during flight muscle development in Drosophila. The generality of the method makes it suitable for application to other, less well known biological systems for which the temporal organisation of processes plays an important role.

Monarch caterpillars are robust to combined exposure to the roadside micronutrients sodium and zinc.

Human activities are increasing the environmental availability of micronutrients, including sodium and some essential metals. Micronutrients are often limiting in animal diets but may have negative effects when consumed in excess. Though prior research has documented how elevated exposure to individual micronutrients can impact organismal development and fitness, we know less about combined effects of multiple micronutrients. In the wild, monarch butterfly larvae (Danaus plexippus) commonly consume plants in roadside habitats that contain elevated levels of sodium (from road salt) and zinc (from vehicle wear-and-tear). We reared monarch caterpillars to adulthood to test individual and combined effects of dietary sodium and zinc on components of fitness, sodium-linked phenotypes (proxies for neural and flight muscle development) and concentrations of sodium and zinc in adult butterflies. Monarch survival was not impacted by elevated sodium or zinc individually or in combination. Yet, monarchs feeding on sodium-treated milkweed developed relatively larger eyes, consistent with a positive effect of sodium on neural development. Measurements of element concentrations in butterfly and plant tissue indicated that monarchs had higher zinc levels than those present in zinc-treated milkweed but lower sodium levels than those present in sodium-treated milkweed. Monarchs developing on sodium-treated milkweed also had prolonged development time, which might be a cost associated with developing extra neural tissue or investing in mechanisms to excrete excess dietary sodium during the larval stage. Our results indicate that sodium, more than zinc, is likely influencing phenotypic development and performance of insect pollinators in roadside habitats. Yet, in contrast to previous work, our experiment suggests that the highest levels of sodium found along roads are not always harmful for developing monarchs. Future work could consider how potentially stressful effects of micronutrients could be mitigated by increased macronutrient availability or how developmental factors such as migratory status might increase micronutrient requirements.

Analysis of Differentially Expressed Genes of Chrysoperla sinica Related to Flight Capacity by Transcriptome.

The lacewing Chrysoperla sinica (Tjeder) is a common natural enemy of many insect pests in China and is frequently employed for biological control programs. Adults make migratory flights after emergence, which reduces their effectiveness as biological control agents. Previously, we proved that 2-d-old unmated females exhibited significantly stronger flight ability than 3-d-old ones. Meanwhile, 3-d-old unmated adults flew significantly longer distances than mated ones. In this study, Illumina RNA sequencing was performed to characterize differentially expressed genes (DEGs) between virgin and mated adults of different ages in a single female strain of C. sinica. In total, 713,563,726 clean reads were obtained and de novo assembled into 109,165 unigenes with an average length of 847 bp (N50 of 1,754 bp), among which 4,382 (4.01%) unigenes matched known proteins. Based on these annotations, many putative transcripts were related to C. sinica’s flight capacity and muscle structure, energy supply, growth, development, environmental adaptability, and metabolism of nutritional components and bioactive components. In addition, the differential expression of transcripts between different ages and mating status were analyzed, and DEGs participating in flight capacity and muscles were detected, including glutathione hydrolase, NAD-specific glutamate dehydrogenase, aminopeptidase, and acidic amino acid decarboxylase. The DEGs with functions associated with flight capacity and muscles exhibited higher transcript levels for younger (2 d--old) virgins. This comprehensive C. sinica transcriptomic data provide a foundation for a better understanding of the molecular mechanisms underlying the flight capacity to meet the physiological demands of flight muscles in C. sinica.

High-Stakes Decision-Making by Female Crickets (Gryllus texensis): When to Trade In Wing Muscles for Eggs.

AbstractResource-intensive traits, such as dispersal and reproduction, can be difficult to express simultaneously because of resource limitations. One solution is to switch between resource-intensive behaviors. Such phenotypic plasticity is one strategy that organisms use to funnel resources from one expensive trait to another. In crickets (Gryllus texensis), the development and maintenance of flight muscles reduce resource availability for reproduction, leading to physiological trade-offs between the two traits. Long-winged female G. texensis can histolyze their wing muscles, resulting in increased egg production, but they can then no longer fly. Using a diet that mimics food availability in the field, we found that long-winged females adopted one of the three following strategies: early reproduction, intermediate reproduction, and late reproduction. Some late reproducers maintained their flight capability until the end of their natural life span and laid few eggs. If females lost the ability to fly (i.e., their hind wings are removed), they laid eggs earlier, leading to increased reproductive output. However, other environmental cues (e.g., an increased number of mates, increased oviposition substrate quality, or a bout of dispersal flight) had no effect. Late-reproducing females laid 96% fewer eggs than early reproducers, suggesting that late reproduction exacts a huge fitness cost. Nevertheless, some females maintain their flight muscles to the end of their natural life span in both the lab and the field. We suggest that the ability to fly allows for bet hedging against an environmental catastrophe (e.g., drought or flood). This benefit may help explain the persistence of late-reproducing long-winged females, despite the cost of this choice. As climate change increases drought and flood in Texas, late dispersal may be one factor that helps this species survive in the future. An increased understanding of factors that maintain seemingly low fitness strategies can help us predict the resilience of species under climate change.