Functional trade-offs in the limb muscles of dogs selected for running vs. fighting

The physical demands of rapid and economical running differ from those of physical fighting such that functional trade-offs may prevent simultaneous evolution of optimal performance in both behaviours. Here we test three hypotheses of functional trade-off by measuring determinants of limb musculoskeletal function in two breeds of domestic dogs that have undergone intense artificial selection for running (Greyhound) or fighting performance (Pit Bull). We found that Greyhounds differ from Pit Bulls in having relatively less muscle mass distally in their limbs, weaker muscles in their forelimbs than their hindlimbs, and a much greater capacity for elastic storage in the in-series tendons of the extensor muscles of their ankle joints. These observations are consistent with the hypothesis that specialization for rapid or economical running can limit fighting performance and vice versa. We suggest that functional trade-offs that prevent simultaneous evolution of optimal performance in both locomotor and fighting abilities are widespread taxonomically.     

Intraspecific trait variation influences physiological performance and fitness in the South Africa shrub genus Protea (Proteaceae)

Background and AimsGlobal plant trait datasets commonly identify trait relationships that are interpreted to reflect fundamental trade-offs associated with plant strategies, but often these trait relationships are not identified when evaluating them at smaller taxonomic and spatial scales. In this study we evaluate trait relationships measured on individual plants for five widespread Protea species in South Africa to determine whether broad-scale patterns of structural trait (e.g. leaf area) and physiological trait (e.g. photosynthetic rates) relationships can be detected within natural populations, and if these traits are themselves related to plant fitness.MethodsWe evaluated the variance structure (i.e. the proportional intraspecific trait variation relative to among-species variation) for nine structural traits and six physiological traits measured in wild populations. We used a multivariate path model to evaluate the relationships between structural traits and physiological traits, and the relationship between these traits and plant size and reproductive effort.Key ResultsWhile intraspecific trait variation is relatively low for structural traits, it accounts for between 50 and 100 % of the variation in physiological traits. Furthermore, we identified few trait associations between any one structural trait and physiological trait, but multivariate regressions revealed clear associations between combinations of structural traits and physiological performance (R² = 0.37–0.64), and almost all traits had detectable associations with plant fitness.ConclusionsIntraspecific variation in structural traits leads to predictable differences in individual-level physiological performance in a multivariate framework, even though the relationship of any particular structural trait to physiological performance may be weak or undetectable. Furthermore, intraspecific variation in both structural and physiological traits leads to differences in plant size and fitness. These results demonstrate the importance of considering measurements of multivariate phenotypes on individual plants when evaluating trait relationships and how trait variation influences predictions of ecological and evolutionary outcomes.     

Interactions and trade-offs among physiological determinants of performance and reproductive success

How an animal performs in its natural environment ultimately plays a key role in its reproductive success. While a number of studies have investigated how selection acts on performance-related traits, far fewer studies have examined the mechanisms responsible for variation in performance. Among mechanisms, variable morphology has received the most attention. Although physiological traits have received less attention, they are intrinsically related to performance and ultimately to reproductive success. We present a framework whereby investigators can link some basic physiological functions with organismal performance and ultimately with reproductive success. We propose that performance and ultimately reproductive success are strongly influenced by hormones, immune functions, and energetics. We further argue that no physiological function can be considered in isolation and thus our model emphasizes interactions and trade-offs both within each physiological function as well as among them. Some of the most commonly studied trade-offs are between reproduction and immune functions, with energetics as one of the key common currencies for these trade-offs. From an evolutionary perspective, the largest gaps in our knowledge lie in how these interactions and trade-offs influence reproductive success. We believe that a full understanding of how hormones, immune functions, and energetics influence performance traits related to reproduction and, ultimately, lifetime reproductive success requires recognition of the complex relationships, interactions, and trade-offs among these processes.     

Optimal annual routines: behaviour in the context of physiology and ecology

Organisms in a seasonal environment often schedule activities in a regular way over the year. If we assume that such annual routines have been shaped by natural selection then life-history theory should provide a basis for explaining them. We argue that many life-history trade-offs are mediated by underlying physiological variables that act on various time scales. The dynamics of these variables often preclude considering one period of the year in isolation. In order to capture the essence of annual routines, and many life-history traits, a detailed model of changes in physiological state over the annual cycle is required. We outline a modelling approach based on suitable physiological and ecological state variables that can capture this underlying biology, and describe how models based on this approach can be used to generate a range of insights and predictions.     

Trade-offs between plant leaf hydraulic and economic traits

Leaf is the most important organ for carbon-water coupling of a plant because it is the primary medium for photosynthesis. It also acts as the hydraulic bottleneck and safety valve against hydraulic catastrophic dysfunctions. The leaf economics spectrum, which reflects the balance between investments and returns of leaf economic traits, provides a useful framework for examining species strategies as shaped by their evolutionary history. Changes in leaf hydraulic traits will influence leaf economic traits as well as plant survival and growth. Exploring trade-offs between leaf hydraulic and economic traits is thus of significance for modeling carbon-water relations, understanding the mechanisms of water/carbon investments, and extending the leaf economic spectrum. In this review, we first examined the trade-offs between leaf hydraulic and economic traits. Specially, we analyzed the relationships between leaf hydraulic conductivity and hydraulic vulnerability, water potential at the turgor loss point, water capacitance, safety margin, and leaf morphological, structural and functional traits. We then discussed potential mechanisms regulating leaf hydraulic and economic traits from leaf morphology, anatomy, venation, and stomatal functions. Finally, we proposed future research to: (1) develop an integrated whole-plant economics spectrum, including carbon-nitrogen-water resources and root-stem-leaf hydraulic transport system that will help revealing ecophysiological mechanisms of plant structure-functional coupling, carbon sequestration and water use; (2) explore a generalized trade-offs among leaf hydraulic safety, hydraulic efficiency and carbon fixation efficiency to advance our understanding of the relationships between biophysical structure and physiological metabolism in plant leaf construction under drought stress; and (3) explore the carbon-water metabolic relationship and coupling of water transport and growth rate for the metabolic theory and predictions at community scale.     

植物叶片水力与经济性状权衡关系的研究进展

叶片既是植物光合产物形成的主要场所, 又是整株植物的水力瓶颈、应对灾难性水力失调的安全阀门, 是植物碳水耦合权衡的重要器官。叶经济型谱反映了叶片经济性状“投资-收益”的权衡, 为验证植物进化过程中形成的物种对策提供了适用的理论框架。叶片水力性状变化会影响叶片经济性状及植物存活和生长。因此, 探索植物叶片水力与经济性状的权衡关系, 对建立植物碳-水耦合模型、揭示植物水-碳投资机理、扩展植物性状型谱等均有重要意义。该文首先综述了叶片水力性状、经济性状及两者之间的权衡关系, 分析了叶片导水率与水力脆弱性、失膨点水势、水容、安全阈值等水力性状以及与叶片的形态、结构和气体交换功能性状之间的关系。然后, 从叶片形态、解剖和叶脉网络结构以及气孔功能方面探讨了叶片水力性状与经济性状的调节机制。最后, 提出今后应加强三方面的研究: (1)探索建立植物根-茎-叶水力输导系统的碳-氮-水资源的整株经济型谱, 以揭示植物功能结构耦合、高效固碳用水的生理生态学机制; (2)探索叶片水力安全、水力效率和固碳效率之间的普适性权衡关系, 以深入理解抗旱植物叶片构建的生物物理结构与生理代谢的关系; (3)探索个体水平碳水代谢关系、水分运输与生长速率的耦合, 为代谢推演理论和植物群落尺度预测提供基础。     

Trade-offs between the reproductive and immune systems: facultative responses to resources or obligate responses to reproduction?

A major challenge in biology is understanding how organisms partition limited resources among physiological processes. For example, offspring production and self-maintenance are important for fitness and survival, yet these critical processes often compete for resources. While physiological trade-offs between reproduction and immune function have been documented, their regulation remains unclear. Most current evidence suggests that physiological changes during specific reproductive states directly suppress various components of the immune system; however, some studies have not found this clear relationship. We performed two experiments in female tree lizards (Urosaurus ornatus) that demonstrate the presence of trade-offs between the reproductive and immune systems under controlled laboratory conditions. These results also support the hypothesis that these trade-offs are a facultative response to resource availability and are not obligatory responses to physiological changes during reproduction. We found that (1) experimentally increasing reproductive investment under limited resources resulted in suppressed immune function and (2) experimentally limiting resources resulted in immunosuppression but only during resource costly reproductive activities. There seems to be a critical balance of resources that is maintained between multiple processes, and changes in the balance between energy intake and output can have major consequences for immune function.     

Constraints on muscular performance: trade-offs between power output and fatigue resistance

An important functional and evolutionary constraint on the physical performance of vertebrates is believed to be the trade-off between speed and endurance capacity. However, despite the pervasiveness of physiological arguments, most studies have found no evidence of the trade-off when tested at the whole-animal level. We investigated the existence of this trade-off at the whole-muscle level, the presumed site of this physiological conflict, by examining inter-individual variation in both maximum power output and fatigue resistance for mouse extensor digitorum longus (EDL) muscle using the work-loop technique. We found negative correlations between several measures of in vitro maximum power output and force production with fatigue resistance for individual mouse EDL muscles, indicating functional trade-offs between these performance parameters. We suggest that this trade-off detected at the whole-muscle level has imposed an important constraint on the evolution of vertebrate physical performance.     

Nutritional requirements for web synthesis in the tetragnathid spider Nephila clavipes

Trap-constructing organisms provide a unique opportunity for the study of resource allocation, because an observer can unambiguously determine the allocation to foraging. In species that synthesize a trap from physiologically important compounds, there is the further advantage that there may be direct trade-offs between allocation of resources to foraging and physiological functions. We examined the ability of the spider Nephila clavipes (L.; Araneae: Tetragnathidae) to synthesize resources that are known to be used for both web synthesis and non-foraging physiological functions. We found that choline, required for both web function and physiological function, is an essential nutrient: it is not synthesized by this spider. Under laboratory conditions with a diet of fruit flies, choline is limiting, and the spiders make allocation trade-offs between investing choline in foraging (the web) or in their body.     

The impact of experimentally elevated energy expenditure on oxidative stress and lifespan in the short-tailed field vole Microtus agrestis

Life-history theory assumes that animal life histories are a consequence of trade-offs between current activities and future reproductive performance or survival, because resource supply is limited. Empirical evidence for such trade-offs in the wild are common, yet investigations of the underlying mechanisms are rare. Life-history trade-offs may have both physiological and ecological mediated costs. One hypothesized physiological mechanism is that elevated energy metabolism may increase reactive oxygen species production, leading to somatic damage and thus compromising future survival. We investigated the impact of experimentally elevated energy expenditure on oxidative damage, protection and lifespan in short-tailed field voles (Microtus agrestis) maintained in captivity to remove any confounding ecological factor effects. Energy expenditure was elevated via lifelong cold exposure (7+/-2 degrees C), relative to siblings in the warm (22+/-2 degrees C). No treatment effect on cumulative mortality risk was observed, with negligible effects on oxidative stress and antioxidant protection. These data suggest that in captive animals physiologically mediated costs on life history do not result from increased energy expenditure and consequent elevations in oxidative stress and reduced survival.     

Leptin as a physiological mediator of energetic trade-offs in ecoimmunology: implications for disease

Organisms must distribute sufficient energy among different and often competing physiological systems. This task can become challenging, however, as resources are often limiting, resulting in energetic trade-offs. For example, energetically based trade-offs between the reproductive and immune systems are common across taxa, yet the regulatory mechanisms underlying these trade-offs remain unclear. The adipose tissue hormone leptin is an ideal candidate for the modulation of energetic trade-offs between different physiological systems as this hormone serves as a gage of fat reserves and also modulates a range of physiological activities including the reproductive and immune processes. This article presents a review of the evidence for the role of leptin as a modulator of energetic trade-offs with the immune system and suggests its importance in disease ecology. In addition, we provide a case study of the ornate tree lizard (Urosaurus ornatus), testing whether leptin is involved in mediating a well-documented influence of energy state on the trade-off between reproductive activity and immune function. Overall, the combined results suggest that leptin serves as a proximate endocrine signal of available energy to the immune system, and therefore likely to affect susceptibility to diseases.     

Sex-specific development of avian flight performance under experimentally altered rearing conditions

Numerous studies have examined predation risk resulting fromthe costs of impaired flight performance associated with manykey life-history stages such as reproduction and migration.Interestingly, although avian nestlings experience multipleresource-based physiological trade-offs and undergo considerablemorphological and physiological changes during postnatal development,there is no data available on how nestlings manage the competingdemands of growth and the development of flight ability at thiscritical life-history stage. We examined numerous morphologicaltraits to determine which are responsible for variation in flightperformance in juvenile European starlings (Sturnus vulgaris),a sexually size-dimorphic passerine. We then manipulated maternalquality during chick rearing (via feather clipping) to examinesex-specific sensitivity of fledgling flight performance tothe quality of the rearing environment. Results suggest thatthe mechanics underlying variation in juvenile flight performanceare relatively simple, being principally determined by the ratioof pectoral muscle mass to body mass (BM) and the surface areaof the wings. Interestingly, although the maternal quality manipulationdecreased BM and structural size in daughters, only the flightperformance of sons was negatively affected. Our results suggestthat a survival-related trait can be significantly affectedin the larger sex when raised under stressful conditions. Furthermore,measuring only BM and structural size may not be sufficientin understanding how the sexes are affected by stressful rearingconditions in sexually size-dimorphic species.     

Regulation of male traits by testosterone: implications for the evolution of vertebrate life histories

The negative co-variation of life-history traits such as fecundity and lifespan across species suggests the existence of ubiquitous trade-offs. Mechanistically, trade-offs result from the need to differentially allocate limited resources to traits like reproduction versus self-maintenance, with selection favoring the evolution of optimal allocation mechanism. Here I discuss the physiological (endocrine) mechanisms that underlie optimal allocation rules and how such rules evolve. The hormone testosterone may mediate life-history trade-offs due to its pleiotropic actions in male vertebrates. Conservation in the actions of testosterone in vertebrates has prompted the 'evolutionary constraint hypothesis,' which assumes that testosterone signaling mechanisms and male traits evolve as a unit. This hypothesis implies that the actions of testosterone are similar across sexes and species, and only the levels of circulating testosterone concentrations change during evolution. In contrast, the 'evolutionary potential hypothesis' proposes that testosterone signaling mechanisms and male traits evolve independently. In the latter scenario, the linkage between hormone and traits itself can be shaped by selection, leading to variation in trade-off functions. I will review recent case studies supporting the evolutionary potential hypothesis and suggest micro-evolutionary experiments to unravel the mechanistic basis of life-history evolution.     

Explaining Dog Wolf Differences in Utilizing Human Pointing Gestures: Selection for Synergistic Shifts in the Development of Some Social Skills

Background

The comparison of human related communication skills of socialized canids may help to understand the evolution and the epigenesis of gesture comprehension in humans. To reconcile previously contradicting views on the origin of dogs'' outstanding performance in utilizing human gestures, we suggest that dog-wolf differences should be studied in a more complex way.

Methodology/Principal Findings

We present data both on the performance and the behaviour of dogs and wolves of different ages in a two-way object choice test. Characteristic behavioural differences showed that for wolves it took longer to establish eye contact with the pointing experimenter, they struggled more with the handler, and pups also bit her more before focusing on the human''s signal. The performance of similarly hand-reared 8-week-old dogs and wolves did not differ in utilizing the simpler proximal momentary pointing. However, when tested with the distal momentary pointing, 4-month-old pet dogs outperformed the same aged hand reared wolves. Thus early and intensive socialisation does not diminish differences between young dogs and wolves in behaviour and performance. Socialised adult wolves performed similarly well as dogs in this task without pretraining. The success of adult wolves was accompanied with increased willingness to cooperate.

Conclusion/Significance

Thus, we provide evidence for the first time that socialised adult wolves are as successful in relying on distal momentary pointing as adult pet dogs. However, the delayed emergence of utilising human distal momentary pointing in wolves shows that these wild canines react to a lesser degree to intensive socialisation in contrast to dogs, which are able to control agonistic behaviours and inhibition of actions in a food related task early in development. We suggest a “synergistic” hypothesis, claiming that positive feedback processes (both evolutionary and epigenetic) have increased the readiness of dogs to attend to humans, providing the basis for dog-human communication.     

Triturus newts defy the running-swimming dilemma

Conflicts between structural requirements for carrying out different ecologically relevant functions may result in a compromise phenotype that maximizes neither function. Identifying and evaluating functional trade-offs may therefore aid in understanding the evolution of organismal performance. We examined the possibility of an evolutionary trade-off between aquatic and terrestrial locomotion in females of European species of the newt genus Triturus. Biomechanical models suggest a conflict between the requirements for aquatic and terrestrial locomotion. For instance, having an elongate, slender body, a large tail, and reduced limbs should benefit undulatory swimming, but at the cost of reduced running capacity. To test the prediction of an evolutionary trade-off between swimming and running capacity, we investigated relationships between size-corrected morphology and maximum locomotor performance in females of ten species of newts. Phylogenetic comparative analyses revealed that an evolutionary trend of body elongation (increasing axilla-groin distance) is associated with a reduction in head width and forelimb length. Body elongation resulted in reduced maximum running speed, but, surprisingly, also led to a reduction in swimming speed. The evolution of longer tails was associated with an increase in maximal swimming speed. We found no evidence for an evolutionary trade-off between aquatic and terrestrial locomotor performance, probably because of the unexpected negative effect of body elongation on swimming speed. We conclude that the idea of a design conflict between aquatic and terrestrial locomotion, mediated through antagonistic effects of body elongation, does not apply to our model system.     

Running energetics of the North American river otter: do short legs necessarily reduce efficiency on land?

Semi-aquatic mammals move between two very different media (air and water), and are subject to a greater range of physical forces (gravity, buoyancy, drag) than obligate swimmers or runners. This versatility is associated with morphological compromises that often lead to elevated locomotor energetic costs when compared to fully aquatic or terrestrial species. To understand the basis of these differences in energy expenditure, this study examined the interrelationships between limb morphology, cost of transport and biomechanics of running in a semi-aquatic mammal, the North American river otter. Oxygen consumption, preferred locomotor speeds, and stride characteristics were measured for river otters (body mass=11.1 kg, appendicular/axial length=29%) trained to run on a treadmill. To assess the effects of limb length on performance parameters, kinematic measurements were also made for a terrestrial specialist of comparable stature, the Welsh corgi dog (body mass=12.0 kg, appendicular/axial length=37%). The results were compared to predicted values for long legged terrestrial specialists. As found for other semi-aquatic mammals, the net cost of transport of running river otters (6.63 J kg(-1)min(-1) at 1.43 ms(-1)) was greater than predicted for primarily terrestrial mammals. The otters also showed a marked reduction in gait transition speed and in the range of preferred running speeds in comparison to short dogs and semi-aquatic mammals. As evident from the corgi dogs, short legs did not necessarily compromise running performance. Rather, the ability to incorporate a period of suspension during high speed running was an important compensatory mechanism for short limbs in the dogs. Such an aerial period was not observed in river otters with the result that energetic costs during running were higher and gait transition speeds slower for this versatile mammal compared to locomotor specialists.     

Consequences of metamorphosis for the locomotor performance and thermal physiology of the newt Triturus cristatus

During metamorphosis, most amphibians undergo rapid shifts in their morphology that allow them to move from an aquatic to a more terrestrial existence. Two important challenges associated with this shift in habitat are the necessity to switch from an aquatic to terrestrial mode of locomotion and changes in the thermal environment. In this study, I investigated the consequences of metamorphosis to the burst swimming and running performance of the European newt Triturus cristatus to determine the nature and magnitude of any locomotor trade-offs that occur across life-history stages. In addition, I investigated whether there were any shifts in the thermal dependence of performance between life-history stages of T. cristatus to compensate for changes in their thermal environment during metamorphosis. A trade-off between swimming and running performance was detected across life-history stages, with metamorphosis resulting in a simultaneous decrease in swimming and increase in running performance. Although the terrestrial habitat of postmetamorphic stages of the newt T. cristatus experienced greater daily fluctuations in temperature than the aquatic habitat of the larval stage, no differences in thermal sensitivity of locomotor performance were detected between the larval aquatic and postmetamorphic stages. The absence of variation across life-history stages of T. cristatus may indicate that thermal sensitivity may be a conservative trait across ontogenetic stages in amphibians, but further studies are required to investigate this assertion.     

Seroprevalence of Neospora caninum antibodies in dogs in India

Neospora caninum is one of most important causes of abortion in cattle worldwide, and dogs are an important risk factor for N. caninum infection in cattle. Antibodies to N. caninum were determined in 184 (126 rural, 58 urban) dogs from the Punjab State, India, using commercial monoclonal antibody-based competitive ELISA and found in 16.8% of the animals. The prevalence of N. caninum antibodies was significantly higher in rural dogs (21.4%, 27 of 126) than city dogs (6.9%, 4 of 58). To our knowledge this is the first report of N. caninum infection in canines from India.     

An SNP within the angiotensin-converting enzyme distinguishes between sprint and distance performing Alaskan sled dogs in a candidate gene analysis

The Alaskan sled dog offers a unique mechanism for studying the genetics of elite athletic performance. They are a group of mixed breed dogs, comprised of multiple common breeds, and a unique breed entity seen only as a part of the sled dog mix. Alaskan sled dogs are divided into 2 primary groups as determined by their racing skills. Distance dogs are capable of running over 1000 miles in 10 days, whereas sprint dogs run much shorter distances, approximately 30 miles, but in faster times, that is, 18-25 mph. Finding the genes that distinguish these 2 types of performers is likely to illuminate genetic contributors to human athletic performance. In this study, we tested for association between polymorphisms in 2 candidate genes; angiotensin-converting enzyme (ACE) and myostatin (MSTN) and enhanced speed and endurance performance in 174 Alaskan sled dogs. We observed 81 novel genetic variants within the ACE gene and 4 within the MSTN gene, including a polymorphism within the ACE gene that significantly (P value 2.38 × 10(-5)) distinguished the sprint versus distance populations.     

Reactive oxygen species as universal constraints in life-history evolution

Evolutionary theory is firmly grounded on the existence of trade-offs between life-history traits, and recent interest has centred on the physiological mechanisms underlying such trade-offs. Several branches of evolutionary biology, particularly those focusing on ageing, immunological and sexual selection theory, have implicated reactive oxygen species (ROS) as profound evolutionary players. ROS are a highly reactive group of oxygen-containing molecules, generated as common by-products of vital oxidative enzyme complexes. Both animals and plants appear to intentionally harness ROS for use as molecular messengers to fulfil a wide range of essential biological processes. However, at high levels, ROS are known to exert very damaging effects through oxidative stress. For these reasons, ROS have been suggested to be important mediators of the cost of reproduction, and of trade-offs between metabolic rate and lifespan, and between immunity, sexual ornamentation and sperm quality. In this review, we integrate the above suggestions into one life-history framework, and review the evidence in support of the contention that ROS production will constitute a primary and universal constraint in life-history evolution.