Locomotor effects of a fibrosis-based immune response in stickleback fish.

The vertebrate immune system provides an impressively effective defense against parasites and pathogens. However, these benefits must be balanced against a range of costly side-effects including energy loss and risks of auto-immunity. These costs might include biomechanical impairment of movement, but little is known about the intersection between immunity and biomechanics. Here, we show that a fibrosis immune response to Schistocephalus solidus infection in freshwater threespine stickleback (Gasterosteus aculeatus) has collateral effects on their locomotion. Although fibrosis is effective at reducing infection, some populations of stickleback actively suppress this immune response, possibly because the costs of fibrosis outweigh the benefits. We quantified the locomotor effects of the fibrosis immune response in the absence of parasites to investigate whether there are incidental costs of fibrosis that could help explain why some fish forego this effective defense. To do this, we induced fibrosis in stickleback and then tested their C-start escape performance. Additionally, we measured the severity of fibrosis, body stiffness and body curvature during the escape response. We were able to estimate performance costs of fibrosis by including these variables as intermediates in a structural equation model. This model revealed that among control fish without fibrosis, there is a performance cost associated with increased body stiffness. However, fish with fibrosis did not experience this cost but rather displayed increased performance with higher fibrosis severity. This result demonstrates that the adaptive landscape of immune responses can be complex with the potential for wide-reaching and unexpected fitness consequences.

Trophic niche drives the evolution of craniofacial shape in Trinidadian guppies.

Diverse clades of fishes adapted to feeding on the benthos repeatedly converge on steep craniofacial profiles and shorter, wider heads. But in an incipient radiation, to what extent is this morphological evolution measurable and can we distinguish the relative genetic vs. plastic effects? We use the Trinidadian guppy (Poecilia reticulata) to test the repeatability of adaptation and the alignment of genetic and environmental effects shaping poecilid craniofacial morphology. We compare wild-caught and common garden lab-reared fish to quantify the genetic and plastic components of craniofacial morphology across 4 populations from 2 river drainage systems (n = 56 total). We first use micro-computed tomography to capture 3D morphology, then place both landmarks and semilandmarks to perform size-corrected 3D morphometrics and quantify shape space. We find a measurable, significant, and repeatable divergence in craniofacial shape between high-predation invertivore and low-predation detritivore populations. As predicted from previous examples of piscine adaptive trophic divergence, we find increases in head slope and craniofacial compression among the benthic detritivore foragers. Furthermore, the effects of environmental plasticity among benthic detritivores produce exaggerated craniofacial morphological change along a parallel axis to genetic morphological adaptation from invertivore ancestors. Overall, many of the major patterns of benthic-limnetic craniofacial evolution appear convergent among disparate groups of teleost fishes.

Genes, Morphology, Performance, and Fitness: Quantifying Organismal Performance to Understand Adaptive Evolution.

To understand the complexities of morphological evolution, we must understand the relationships between genes, morphology, performance, and fitness in complex traits. Genomicists have made tremendous progress in finding the genetic basis of many phenotypes, including a myriad of morphological characters. Similarly, field biologists have greatly advanced our understanding of the relationship between performance and fitness in natural populations. However, the connection from morphology to performance has primarily been studied at the interspecific level, meaning that in most cases we lack a mechanistic understanding of how evolutionarily relevant variation among individuals affects organismal performance. Therefore, functional morphologists need methods that will allow for the analysis of fine-grained intraspecific variation in order to close the path from genes to fitness. We suggest three methodological areas that we believe are well suited for this research program and provide examples of how each can be applied within fish model systems to build our understanding of microevolutionary processes. Specifically, we believe that structural equation modeling, biological robotics, and simultaneous multi-modal functional data acquisition will open up fruitful collaborations among biomechanists, evolutionary biologists, and field biologists. It is only through the combined efforts of all three fields that we will understand the connection between evolution (acting at the level of genes) and natural selection (acting on fitness).

Locomotor effects of a fibrosis-based immune response in stickleback fish.

The vertebrate immune system provides an impressively effective defense against parasites and pathogens. However, these benefits must be balanced against a range of costly side-effects including energy loss and risks of auto-immunity. These costs might include biomechanical impairment of movement, but little is known about the intersection between immunity and biomechanics. Here, we show that a fibrosis immune response in threespine stickleback (Gasterosteus aculeatus) has collateral effects on their locomotion. When freshwater stickleback are infected with the tapeworm parasite Schistocephalus solidus, they face an array of fitness consequences ranging from impaired body condition and fertility to an increased risk of mortality. To fight the infection, some stickleback will initiate a fibrosis immune response in which they produce excess collagenous tissue in their coelom. Although fibrosis is effective at reducing infection, some populations of stickleback actively suppress this immune response, possibly because the costs of fibrosis outweigh the benefits. Here we quantify the locomotor effects of the fibrosis immune response in the absence of parasites to investigate whether there are collateral costs of fibrosis that could help explain why some fish forego this effective defense. To do this, we induce fibrosis in stickleback and then test their C-start escape performance. Additionally, we measure the severity of fibrosis, body stiffness, and body curvature during the escape response. We were able to estimate performance costs of fibrosis by including these variables as intermediates in a structural equation model. This model reveals that among control fish without fibrosis, there is a performance cost associated with increased body stiffness. However, fish with fibrosis did not experience this cost but rather displayed increased performance with higher fibrosis severity. This result demonstrates that the adaptive landscape of immune responses can be complex with the potential for wide reaching and unexpected fitness consequences.

Role of the caudal peduncle in a fish-inspired robotic model: how changing stiffness and angle of attack affects swimming performance.

In fish, the tail is a key element of propulsive anatomy that contributes to thrust during swimming. Fish possess the ability to alter tail stiffness, surface area and conformation. Specifically, the region at the base of the tail, the caudal peduncle, is proposed to be a key location of fish stiffness modulation during locomotion. Most previous analyses have focused on the overall body or tail stiffness, and not on the effects of changing stiffness specifically at the base of the tail in fish and robotic models. We used both computational fluid dynamics analysis and experimental measurements of propulsive forces in physical models with different peduncle stiffnesses to analyze the effect of altering stiffness on the tail angle of attack and propulsive force and efficiency. By changing the motion program input to the tail, we were able to alter the phase relationship between the front and back tail sections between 0° and 330°. Computational simulations showed that power consumption was nearly minimized and thrust production was nearly maximized at the kinematic pattern whereφ= 270°, the approximate phase lag observed in the experimental foils and in free swimming tuna. We observed reduced thrust and efficiency at high angles of attack, suggesting that the tail driven during these motion programs experiences stalling and loss of lift. However, there is no single peduncle stiffness that consistently maximizes performance, particularly in physical models. This result highlights the fact that the optimal caudal peduncle stiffness is highly context dependent. Therefore, incorporating the ability to control peduncle stiffness in future robotic models of fish propulsion promises to increase the ability of robots to approach the performance of fish.

An autonomously swimming biohybrid fish designed with human cardiac biophysics.

Biohybrid systems have been developed to better understand the design principles and coordination mechanisms of biological systems. We consider whether two functional regulatory features of the heart-mechanoelectrical signaling and automaticity-could be transferred to a synthetic analog of another fluid transport system: a swimming fish. By leveraging cardiac mechanoelectrical signaling, we recreated reciprocal contraction and relaxation in a muscular bilayer construct where each contraction occurs automatically as a response to the stretching of an antagonistic muscle pair. Further, to entrain this closed-loop actuation cycle, we engineered an electrically autonomous pacing node, which enhanced spontaneous contraction. The biohybrid fish equipped with intrinsic control strategies demonstrated self-sustained body-caudal fin swimming, highlighting the role of feedback mechanisms in muscular pumps such as the heart and muscles.

Fin-fin interactions during locomotion in a simplified biomimetic fish model.

Fish median fins are extremely diverse, but their function is not yet fully understood. Various biological studies on fish and engineering studies on flapping foils have revealed that there are hydrodynamic interactions between fins arranged in tandem and that these interactions can lead to improved performance by the posterior fin. This performance improvement is often driven by the augmentation of a leading-edge vortex on the trailing fin. Past experimental studies have necessarily simplified fish anatomy to enable more detailed engineering analyses, but such simplifications then do not capture the complexities of an undulating fish-like body with fins attached. We present a flexible fish-like robotic model that better represents the kinematics of swimming fishes while still being simple enough to examine a range of morphologies and motion patterns. We then create statistical models that predict the individual effects of each kinematic and morphological variable. Our results demonstrate that having fins arranged in tandem on an undulating body can lead to more steady production of thrust forces determined by the distance between the fins and their relative motion. We find that these same variables also affect swimming speed. Specifically, when swimming at high frequencies, self-propelled speed decreases by 12%-26% due to out of phase fin motion. Flow visualization reveals that variation within this range is caused in part by fin-fin flow interactions that affect leading edge vortices. Our results indicate that undulatory swimmers should optimize both the positioning and relative motion of their median fins in order to reduce force oscillations and improve overall performance while swimming.

Effect of craniofacial genotype on the relationship between morphology and feeding performance in cichlid fishes.

The relationship between morphology and performance is complex, but important for understanding the adaptive nature of morphological variation. Recent studies have sought to better understand this system by illuminating the interconnectedness of different functional systems; however, the role of genetics is often overlooked. In this study, we attempt to gain insights into this relationship by examining the effect of genotypic variation at putative craniofacial loci on the relationship between morphology and feeding performance in cichlids. We studied two morphologically disparate species, as well as a morphologically intermediate hybrid population. We assessed feeding performance, jaw protrusion, and general facial morphology for each fish. We also genotyped hybrid animals at six previously identified craniofacial loci. Cichlid species were found to differ in facial geometry, kinematic morphology, and performance. Significant correlations were also noted between these variables; however, the explanatory power of facial geometry in predicting performance was relatively poor. Notably, when hybrids were grouped by genotype, the relationship between shape and performance improved. This relationship was especially robust in animals with the specialist allele at sox9b, a well-characterized regulator of craniofacial development. These data suggest a novel role for genotype in influencing complex relationships between form and function.