Journal of Experimental Biology最新文献

Symbiotic interactions, central to most life on Earth, are interwoven associations that vary in intimacy and duration. Some of the most well-known examples of symbioses occur between animals and gut bacteria. These associations lead to physiological integration of host and symbionts. The diversity of microbes within animal hosts can make studying them technically challenging. Thus, most science heavily focuses on the animal side of symbioses, limiting study of the microbial symbionts to characterization of their genetic and functional diversity. These limitations are minimized in Heteropteran insects that have specialized midguts that separately house single symbiont species away from ingested food. These insect-bacteria associations allow us to address fundamental questions regarding how both hosts and symbionts change to establish a cooperative relationship. In this study, through ex vivo and in vivo observations of cellular behaviors, we explore concurrent structural and cellular dynamics in both the squash bug host (Anasa tristis) and its Caballeronia zhejiangensis symbionts during the initiation of symbiosis. We elucidate how C. zhejiangensis is sequestered within a specialized symbiotic organ within the A. tristis midgut, how the symbiont uses active motility to reach the symbiotic organ, how symbionts colonize host crypts within the organ and how host crypt morphogenesis progresses during the initiation of symbiotic interactions. Our findings provide insight into how dynamic cellular activity and morphological development reciprocally change in both host and symbiont as they establish symbiotic interactions.

The contribution of the gut to the ingestion, production, absorption and excretion of the extra ammonia and urea nitrogen (urea-N) associated with feeding ('exogenous' fraction) has received limited attention. Analysis of commercial pellet food revealed appreciable concentrations of ammonia and urea-N. Long-term satiation feeding increased whole-trout ammonia and urea-N excretion rates by 2.5-fold above fasting levels. Blood was sampled from the dorsal aorta, posterior, mid- and anterior sub-intestinal veins, as well as the hepatic portal vein in situ. Ammonia, urea-N and fluid flux rates were measured in vitro using novel gut sac preparations filled with native chyme. The sacs maintained the extreme physico-chemical conditions of the lumen seen in vivo. Overall, these results confirmed our hypothesis that the stomach, and anterior intestine and pyloric caecae regions play important roles in ammonia and urea-N production and/or absorption. There was a very high rate of urea-N production in the anterior intestine and pyloric caecae, whereas the posterior intestine dominated for ammonia synthesis. The stomach was the major site of ammonia absorption, and the anterior intestine and pyloric caecae region dominated for urea-N absorption. Model calculations indicated that over 50% of the exogenous ammonia and urea-N excretion associated with satiation feeding was produced in the anaerobic gut. This challenges standard metabolic theory used in fuel-use calculations. The novel gut sac preparations gained fluid during incubation, especially in the anterior intestine and pyloric caecae, owing to marked hyperosmolality in the chyme. Thus, satiation feeding with commercial pellets is beneficial to the water balance of freshwater trout.

Acidification is a key component of digestion throughout metazoans. The gut digestive fluid of many invertebrates is acidified by the vesicular-type H+-ATPase (VHA). In contrast, vertebrates generate acidic gut fluids using the gastric H+/K+-ATPase (HKA), an evolutionary innovation linked with the appearance of a true stomach that greatly improves digestion, absorption and immune function. Hagfishes are the most basal extant vertebrates, and their mechanism of digestive acidification remains unclear. Herein, we report that the stomachless Pacific hagfish (Eptatretus stoutii) acidify their gut using the VHA, and searches of E. stoutii gut transcriptomes and the genome of a closely related hagfish species (E. burgerii) indicate they lack HKA, consistent with its emergence following the 2R whole-genome duplication. Immunostaining revealed prominent VHA presence in the apical membrane of enterocytes and sub-apical expression of both VHA and soluble adenylyl cyclase. Interestingly, akin to vertebrates, VHA was also observed in immature pancreatic-like zymogen granules and was noticeably absent from the mature granules. Furthermore, isolated gut sacs from fed hagfish demonstrate increased VHA-dependent luminal H+ secretion that is stimulated by the cAMP pathway. Overall, these results suggest that the hagfish gut shares the trait of VHA-dependent acidification with invertebrates, while simultaneously performing some roles of the pancreas and intestine of gnathostomes.

An animal's immune function is vital for survival and potentially metabolically expensive, but some pathogens could manipulate their hosts' immune and metabolic responses. One example is Mycoplasma gallisepticum (MG), which infects both the respiratory system and conjunctiva of the eye in house finches (Haemorhous mexicanus). MG has been shown to exhibit immune- and metabolic-suppressive properties, but the physiological mechanisms are still unknown. Recent studies demonstrated that mitochondria could serve as powerhouses for both ATP production and immunity, notably inflammatory processes, through regulating complex II and its metabolites. Consequently, in this study, we investigate the short-term (3d post-inoculation) and long-term (34d post-inoculation) effects of MG infection on the hepatic mitochondrial respiration of house finches from two populations infected with two different MG isolates. After short-term infection, MG-infected birds had significantly lower state 2 and state 4 respiration, but only when using complex II substrates. After long-term infection, MG-infected birds exhibited lower state 3 respiration with both complex I and II substrates, resulting in lower respiratory control ratio compared to uninfected controls, which aligned with the hypothesized metabolic-suppressive properties of MG. Interestingly, there were limited differences in mitochondrial respiration regardless of house finch population of origin, MG isolate, and whether birds recovered from infection or not. We propose that MG may target mitochondrial complex II for its immune-suppressive properties during the early stages of infection and inhibit mitochondrial respiration for its metabolic-suppressive properties at later stage of infection, both of which should delay recovery of the host and extend infectious periods.

Skeletal joint morphology and mobility underlie movement, behavior, and ecology in vertebrates. Joints can be categorized by their shape and articulation type, but such schemes might be unreliable for inferring function across the full diversity of vertebrates. We test hypothesized relationships between joint form and function by collecting marker-based ex vivo, cadaveric XROMM data on the shoulder and elbow joints of the tegu lizard (Salvator merianae) and Virginia opossum (Didelphis virginiana), which between them contain articulations historically classified as ball-and-socket, hemi-sellar, hinge and condylar joints. We measured 3D rotational and translational mobility at each joint and compared our experimental results against predictions based on articular morphology. Contrary to our predictions, the opossum ball-and-socket shoulder joint was less mobile- it had a smaller 3D range of motion envelope- than the tegu hemi-sellar shoulder joint and even the tegu condylar elbow joint, challenging the notion that ball-and-socket shoulder provides an inherent mobility advantage. However, the ball-and-socket opossum shoulder also had a less complex mobility envelope, with fewer interactions between degrees of freedom, allowing it to transition between poses more easily. Matching osteological predictions, the hinge elbow of the opossum was the least mobile. All joints exhibited coupling between rotational and translational degrees of freedom, and we further emphasize the need to incorporate translational motion and soft tissue constraints for accurately modelling joint mobility. Our findings underscore the complexity of form-function relationships in vertebrate skeletal joints, and demonstrate that joint morphology alone, in the absence of soft tissues, does not provide a complete picture of joint mobility.

Quantifying energy costs of various activities is critical to understand key aspects of animal behavior and ecology. Currently, calorimetry is the most widely used method to measure those costs in laboratory studies, whereas field studies use the doubly labeled water method, heart rate, and dynamic body acceleration (DBA). However, these methods are limited or even biased due to restricted space for movement, low temporal resolution, and/or the need for logger attachment or implantation. Measuring energy costs of behaviors is difficult, especially in small, highly mobile animals. Here, using a damselfish, Chromis viridis, we demonstrate that DBA, obtained from marker-less, automatic video tracking and 3D reconstruction, can effectively estimate oxygen consumption rate. We show that our video-based DBA method can be used to estimate metabolic costs of various activities, such as locomotion and feeding, on an individual basis.

Octopuses are known to be visual animals. Beyond functions of the eyes, recent investigations have documented the importance of extraocular photoreception in behavior. Octopus arms have been shown to respond behaviorally to local light exposure with negative phototaxis. Moreover, light-activated chromatophore expansion (LACE) in octopus arms indicates that skin-based photoreception may contribute to light detection. In this study, we used electrophysiological recordings to investigate the neural activity of the arm's axial nerve cord in response to light on the arm. We tested the hypothesis that light stimulates the activity of neurons in the arm's axial nerve cord. We also aimed to determine sensitivity to different wavelengths of light. The results showed that the axial nerve cord is strongly responsive to light stimulation of the arm and that the response travels along the length of the axial nerve cord. Blue light generated the strongest neural activity while red and green light also induced responses. Light-induced neural activity was mediated through the aboral arm skin and by the oral-side skin and suckers. These findings reveal the role of the skin in the sensory abilities of octopuses and provide insights into the neural mechanisms underlying their response to light. Our study underscores the importance of extraocular photoreception in future investigations of cephalopod sensory and behavioral biology.

The activities that define survival and reproductive success in animals depend on their physical performance. However, performance is a complex trait, and organisms must balance competing demands of multiple underlying factors every time they undertake an activity. For example, the morphology that increases bite force (i.e. increased head size) - improving fighting ability - should constrain sprinting performance by adding mass to the body. Consequently, trade-offs between fighting and escape performance might be sex specific where sexual dimorphism is present, or pronounced in animals with extreme breeding strategies. Northern quolls (Dasyurus hallucatus) are a sexually dimorphic marsupial, with sex-specific life history strategies; males die after a single synchronous breeding season, while females can live and breed for 2-3 years. We investigated the effects of sex and life history on whole-animal performance and assessed whether sprint speed and bite force trade off among or within individual male and female quolls. We used a repeated measures dataset spanning 3 years. We identified significant sex differences in morphology and performance, notably after breeding, where male sprint speed decreases but female bite force increases. Both body size and body condition were strong predictors of performance. However, we found no trade-off between sprint speed and bite force, suggesting that ecologically relevant tasks for survival and reproduction - fighting capacity and escape ability - may evolve independently in both male and female northern quolls. Finally, we assessed the repeatability of morphological and performance traits and demonstrated the importance of study design when quantifying variance in animal performance, especially for animals with complex life histories.

The shells of turtles serve as protection, yet shell shape and natural history widely vary among turtles. Here, we identify the mechanical behavior that provides marine turtles, species characterized with fusiform shells, with biomechanical strength and resilience. The multi-layered carapacial bone structure seemingly serves a protective role for the muscles, nerves and viscera it houses. What are the shell's material properties that provide protection? Most previous work has focused on non-marine turtles, which differ in natural history and shell morphology from marine species. We measured carapacial mechanical behavior of green turtle (Chelonia mydas), loggerhead (Caretta caretta) and Kemp's ridleys (Lepidochelys kempii) across a range of body sizes in juveniles, subadults and adults. Carapace samples were tested using quasi-static compression to quantify stiffness (Young's modulus), yield strength and toughness. The mechanical characteristics of marine turtle shells are grossly akin to those of other turtles and driven by the bone's sandwich structure. Yet, the material properties indicate that marine turtle shells are less stiff and strong than those of their freshwater and terrestrial counterparts. We hypothesize that increased flexibility of the shell may reflect tradeoffs for life that include experiencing pressure from diving somewhat deeply in marine environments. Shell material properties also differ among species and ontogenetically. Green turtles have the stiffest, strongest and toughest shells while loggerhead carapaces are the most compliant. Stiffness and yield strength show positive relationships with body size which are most pronounced in green turtles and Kemp's ridleys. Phylogenetic histories and ecological differences likely drive this interspecific variation.

Understanding how muscles use energy is essential for elucidating the role of skeletal muscle in animal locomotion. Yet, experimental measures of in vivo muscle energetics are challenging to obtain, so physiologically based muscle models are often used to estimate energy use. These predictions of individual muscle energy expenditure are not often compared with indirect whole-body measures of energetic cost. Here, we examined and illustrated the capability of physiologically based muscle models to predict in vivo measures of energy use, which rely on fundamental relationships between muscle mechanical state and energy consumption. To improve model predictions and ensure a physiological basis for model parameters, we refined our model to include data from isolated muscle experiments and account for inefficiencies in ATP recovery processes. Simulations were performed to capture three different experimental protocols, which involved varying contraction frequency, duty cycle and muscle fascicle length. Our results demonstrated the ability of the model to capture the dependence of energetic cost on mechanical state across contractile conditions, but tended to underpredict the magnitude of energetic cost. Our analysis revealed that the model was most sensitive to the force-velocity parameters and the data informing the energetic parameters when predicting in vivo energetic rates. This work highlights that it is the mechanics of skeletal muscle contraction that govern muscle energy use, although the precise physiological parameters for human muscle likely require detailed investigation.