Biophysical Determinants and Constraints on Sperm Swimming Velocity.

Over the last 50 years, sperm competition has become increasingly recognised as a potent evolutionary force shaping male ejaculate traits. One such trait is sperm swimming speed, with faster sperm associated with increased fertilisation success in some species. Consequently, sperm are often thought to have evolved to be longer in order to facilitate faster movement. However, despite the intrinsic appeal of this argument, sperm operate in a different biophysical environment than we are used to, and instead increasing length may not necessarily be associated with higher velocity. Here, we test four predictive models (ConstantPower Density, Constant Speed, Constant Power Transfer, Constant Force) of the relationship between sperm length and speed. We collated published data on sperm morphology and velocity from 141 animal species, tested for structural clustering of sperm morphology and then compared the model predictions across all morphologically similar sperm clusters. Within four of five morphological clusters of sperm, we did not find a significant positive relationship between total sperm length and velocity. Instead, in four morphological sperm clusters we found evidence for the Constant Speed model, which predicts that power output is determined by the flagellum and so is proportional to flagellum length. Our results show the relationship between sperm morphology (size, width) and swimming speed is complex and that traditional models do not capture the biophysical interactions involved. Future work therefore needs to incorporate not only a better understanding of how sperm operate in the microfluid environment, but also the importance of fertilising environment, i.e., internal and external fertilisers. The microenvironment in which sperm operate is of critical importance in shaping the relationship between sperm length and form and sperm swimming speed.

Estimation of sinking velocity using free-falling dynamically scaled models: Foraminifera as a test case.

The velocity of settling particles is an important determinant of distribution in extinct and extant species with passive dispersal mechanisms, such as plants, corals and phytoplankton. Here, we adapted dynamic scaling, borrowed from engineering, to determine settling velocity. Dynamic scaling leverages physical models with relevant dimensionless numbers matched to achieve similar dynamics to the original object. Previous studies have used flumes, wind tunnels or towed models to examine fluid flow around objects with known velocities. Our novel application uses free-falling models to determine the unknown sinking velocity of planktonic Foraminifera - organisms important to our understanding of the Earth's current and historic climate. Using enlarged 3D printed models of microscopic Foraminifera tests, sunk in viscous mineral oil to match their Reynolds numbers and drag coefficients, we predicted sinking velocity of real tests in seawater. This method can be applied to study other settling particles such as plankton, spores or seeds.

Microrheology reveals microscale viscosity gradients in planktonic systems.

Microbial activity in planktonic systems creates a dynamic and heterogeneous microscale seascape that harbors a diverse community of microorganisms and ecological interactions of global significance. In recent decades great effort has been put into understanding this complex system, particularly focusing on the role of chemical patchiness, while overlooking a physical parameter that governs microbial life and is affected by biological activity: viscosity. Here we reveal spatial heterogeneity of viscosity in planktonic systems by using microrheological techniques that allow measurement of viscosity at length scales relevant to microorganisms. We show the viscous nature and the spatial extent of the phycosphere, the region surrounding phytoplankton. In ∼45% of the phytoplankton cells analyzed we detected increases in viscosity that extended up to 30 µm away from the cell with up to 40 times the viscosity of seawater. We also show how these gradients of viscosity can be amplified around a lysing phytoplankton cell as its viscous contents leak away. Finally, we report conservative estimates of viscosity inside marine aggregates, hotspots of microbial activity, more than an order of magnitude higher than in seawater. Since the diffusivities of dissolved molecules, particles, and microorganisms are inversely related to viscosity, microheterogeneity in viscosity alters the microscale distribution of microorganisms and their resources, with pervasive implications for the functioning of the planktonic ecosystem. Increasing viscosities impacts ecological interactions and processes, such as nutrient uptake, chemotaxis, and particle encounter, that occur at the microscale but influence carbon and nutrient cycles at a global scale.

150 million years of sustained increase in pterosaur flight efficiency.

The long-term accumulation of biodiversity has been punctuated by remarkable evolutionary transitions that allowed organisms to exploit new ecological opportunities. Mesozoic flying reptiles (the pterosaurs), which dominated the skies for more than 150 million years, were the product of one such transition. The ancestors of pterosaurs were small and probably bipedal early archosaurs1, which were certainly well-adapted to terrestrial locomotion. Pterosaurs diverged from dinosaur ancestors in the Early Triassic epoch (around 245 million years ago); however, the first fossils of pterosaurs are dated to 25 million years later, in the Late Triassic epoch. Therefore, in the absence of proto-pterosaur fossils, it is difficult to study how flight first evolved in this group. Here we describe the evolutionary dynamics of the adaptation of pterosaurs to a new method of locomotion. The earliest known pterosaurs took flight and subsequently appear to have become capable and efficient flyers. However, it seems clear that transitioning between forms of locomotion2,3-from terrestrial to volant-challenged early pterosaurs by imposing a high energetic burden, thus requiring flight to provide some offsetting fitness benefits. Using phylogenetic statistical methods and biophysical models combined with information from the fossil record, we detect an evolutionary signal of natural selection that acted to increase flight efficiency over millions of years. Our results show that there was still considerable room for improvement in terms of efficiency after the appearance of flight. However, in the Azhdarchoidea4, a clade that exhibits gigantism, we test the hypothesis that there was a decreased reliance on flight5-7 and find evidence for reduced selection on flight efficiency in this clade. Our approach offers a blueprint to objectively study functional and energetic changes through geological time at a more nuanced level than has previously been possible.

Rapid decreases in relative testes mass among monogamous birds but not in other vertebrates.

Larger testes produce more sperm and therefore improve reproductive success in the face of sperm competition. Adaptation to social mating systems with relatively high and low sperm competition are therefore likely to have driven changes in relative testes size in opposing directions. Here, we combine the largest vertebrate testes mass dataset ever collected with phylogenetic approaches for measuring rates of morphological evolution to provide the first quantitative evidence for how relative testes mass has changed over time. We detect explosive radiations of testes mass diversity distributed throughout the vertebrate tree of life: bursts of rapid change have been frequent during vertebrate evolutionary history. In socially monogamous birds, there have been repeated rapid reductions in relative testes mass. We see no such pattern in other monogamous vertebrates; the prevalence of monogamy in birds may have increased opportunities for investment in alternative behaviours and physiologies allowing reduced investment in expensive testes.

Motile curved bacteria are Pareto-optimal.

Curved rods are a ubiquitous bacterial phenotype, but the fundamental question of why they are shaped this way remains unanswered. Through in silico experiments, we assessed freely swimming straight- and curved-rod bacteria of a wide diversity of equal-volume shapes parameterized by elongation and curvature, and predicted their performances in tasks likely to strongly influence overall fitness. Performance trade-offs between these tasks lead to a variety of shapes that are Pareto-optimal, including coccoids, all straight rods, and a range of curvatures. Comparison with an extensive morphological survey of motile curved-rod bacteria indicates that the vast majority of species fall within the Pareto-optimal region of morphospace. This result is consistent with evolutionary trade-offs between just three tasks: efficient swimming, chemotaxis, and low cell construction cost. We thus reveal the underlying selective pressures driving morphological diversity in a widespread component of microbial ecosystems.

3D Printing: Applications in evolution and ecology.

In the commercial and medical sectors, 3D printing is delivering on its promise to enable a revolution. However, in the fields of Ecology and Evolution we are only on the brink of embracing the advantages that 3D printing can offer. Here we discuss examples where the process has enabled researchers to develop new techniques, work with novel species, and to enhance the impact of outreach activities. Our aim is to showcase the potential that 3D printing offers in terms of improved experimental techniques, greater flexibility, reduced costs and promoting open science, while also discussing its limitations. By taking a general overview of studies using the technique from fields across the broad range of Ecology and Evolution, we show the flexibility of 3D printing technology and aim to inspire the next generation of discoveries.

Cell morphology governs directional control in swimming bacteria.

The ability to rapidly detect and track nutrient gradients is key to the ecological success of motile bacteria in aquatic systems. Consequently, bacteria have evolved a number of chemotactic strategies that consist of sequences of straight runs and reorientations. Theoretically, both phases are affected by fluid drag and Brownian motion, which are themselves governed by cell geometry. Here, we experimentally explore the effect of cell length on control of swimming direction. We subjected Escherichia coli to an antibiotic to obtain motile cells of different lengths, and characterized their swimming patterns in a homogeneous medium. As cells elongated, angles between runs became smaller, forcing a change from a run-and-tumble to a run-and-stop/reverse pattern. Our results show that changes in the motility pattern of microorganisms can be induced by simple morphological variation, and raise the possibility that changes in swimming pattern may be triggered by both morphological plasticity and selection on morphology.

Independent evolution of shape and motility allows evolutionary flexibility in Firmicutes bacteria.

Functional morphological adaptation is an implicit assumption across many ecological studies. However, despite a few pioneering attempts to link bacterial form and function, functional morphology is largely unstudied in prokaryotes. One intriguing candidate for analysis is bacterial shape, as multiple lines of theory indicate that cell shape and motility should be strongly correlated. Here we present a large-scale use of modern phylogenetic comparative methods to explore this relationship across 325 species of the phylum Firmicutes. In contrast to clear predictions from theory, we show that cell shape and motility are not coupled, and that transitions to and from flagellar motility are common and strongly associated with lifestyle (free-living or host-associated). We find no association between shape and lifestyle, and contrary to recent evidence, no indication that shape is associated with pathogenicity. Our results suggest that the independent evolution of shape and motility in this group might allow a greater evolutionary flexibility.

Density- and trait-mediated effects of a parasite and a predator in a tri-trophic food web.

Despite growing interest in ecological consequences of parasitism in food webs, relatively little is known about effects of parasites on long-term population dynamics of non-host species or about whether such effects are density or trait mediated. We studied a tri-trophic food chain comprised of (i) a bacterial basal resource (Serratia fonticola), (ii) an intermediate consumer (Paramecium caudatum), (iii) a top predator (Didinium nasutum) and (iv) a parasite of the intermediate consumer (Holospora undulata). A fully factorial experimental manipulation of predator and parasite presence/absence was combined with analyses of population dynamics, modelling and analyses of host (Paramecium) morphology and behaviour. Predation and parasitism each reduced the abundance of the intermediate consumer (Paramecium), and parasitism indirectly reduced the abundance of the basal resource (Serratia). However, in combination, predation and parasitism had non-additive effects on the abundance of the intermediate consumer, as well as on that of the basal resource. In both cases, the negative effect of parasitism seemed to be effaced by predation. Infection of the intermediate consumer reduced predator abundance. Modelling and additional experimentation revealed that this was most likely due to parasite reduction of intermediate host abundance (a density-mediated effect), as opposed to changes in predator functional or numerical response. Parasitism altered morphological and behavioural traits, by reducing host cell length and increasing the swimming speed of cells with moderate parasite loads. Additional tests showed no significant difference in Didinium feeding rate on infected and uninfected hosts, suggesting that the combination of these modifications does not affect host vulnerability to predation. However, estimated rates of encounter with Serratia based on these modifications were higher for infected Paramecium than for uninfected Paramecium. A mixture of density-mediated and trait-mediated indirect effects of parasitism on non-host species creates rich and complex possibilities for effects of parasites in food webs that should be included in assessments of possible impacts of parasite eradication or introduction.

Why is eusociality an almost exclusively terrestrial phenomenon?

Eusociality has evolved multiple times across diverse terrestrial taxa, and eusocial species fundamentally shape many terrestrial ecosystems. However, eusocial species are far less common and have much less ecological impact, in aquatic than terrestrial environments. Here, we offer a potential explanation for these observations. It appears that a precondition for the evolution of eusociality is the defence and repeated feeding of offspring in a nest or other protected cavity, and so eusocial species must be able to exploit a predator-safe, long-lasting (multigenerational) expandable nest. We argue that a range of factors mean that opportunities for such nests are much more widespread and the advantages more compelling in terrestrial than aquatic ecosystems.

Relationships between sperm length and speed differ among three internally and three externally fertilizing species.

It is often assumed that longer sperm, by virtue of their increased swimming speed, have a fertilization advantage over shorter sperm when in competition to fertilize eggs. However, there is surprisingly little evidence for a positive correlation between sperm length and speed. Here we use an approach that accounts for within-male variation in sperm traits to examine the relationships between sperm length and sperm speed across a broad range of species, including three internally fertilizing species and three externally fertilizing species. Our results reveal that correlations between sperm size and speed are indeed present and possibly more common than currently thought. However, the direction of the correlations between sperm length and speed, which are more prevalent within a male's ejaculate than among males, were influenced by fertilization mode in contrasting and unexpected ways. Broadly, the patterns revealed that in externally fertilizing species sperm with longer flagellum and shorter heads relative to their flagellum swam faster, whereas in internally fertilizing species sperm with shorter flagellum and longer heads relative to their flagellum swam faster. We discuss these results in light of sperm competition theory and contrast the intraspecific patterns observed in this study with macroevolutionary patterns of sperm evolution reported elsewhere.

Form and metabolic scaling in colonial animals.

Benthic colonial organisms exhibit a wide variation in size and shape and provide excellent model systems for testing the predictions of models that describe the scaling of metabolic rate with organism size. We tested the hypothesis that colony form will influence metabolic scaling and its derivatives by characterising metabolic and propagule production rates in three species of freshwater bryozoans that vary in morphology and module organisation and which demonstrate two- and three-dimensional growth forms. The results were evaluated with respect to predictions from two models for metabolic scaling. Isometric metabolic scaling in two-dimensional colonies supported predictions of a model based on dynamic energy budget theory (DEB) and not those of a model based on fractally branching supply networks. This metabolic isometry appears to be achieved by equivalent energy budgets of edge and central modules, in one species (Cristatella mucedo) via linear growth and in a second species (Lophopus crystallinus) by colony fission. Allometric scaling characterised colonies of a three-dimensional species (Fredericella sultana), also providing support for the DEB model. Isometric scaling of propagule production rates for C. mucedo and F. sultana suggests that the number of propagules produced in colonies increases in direct proportion with the number of modules within colonies. Feeding currents generated by bryozoans function in both food capture and respiration, thus linking metabolic scaling with dynamics of self-shading and resource capture. Metabolic rates fundamentally dictate organismal performance (e.g. growth, reproduction) and, as we show here, are linked with colony form. Metabolic profiles and associated variation in colony form should therefore influence the outcome of biotic interactions in habitats dominated by colonial animals and may drive patterns of macroevolution.

Characteristics and drivers of high-altitude ladybird flight: insights from vertical-looking entomological radar.

Understanding the characteristics and drivers of dispersal is crucial for predicting population dynamics, particularly in range-shifting species. Studying long-distance dispersal in insects is challenging, but recent advances in entomological radar offer unique insights. We analysed 10 years of radar data collected at Rothamsted Research, U.K., to investigate characteristics (altitude, speed, seasonal and annual trends) and drivers (aphid abundance, air temperature, wind speed and rainfall) of high-altitude flight of the two most abundant U.K. ladybird species (native Coccinella septempunctata and invasive Harmonia axyridis). These species cannot be distinguished in the radar data since their reflectivity signals overlap, and they were therefore analysed together. However, their signals do not overlap with other, abundant insects so we are confident they constitute the overwhelming majority of the analysed data. The target species were detected up to ∼1100 m above ground level, where displacement speeds of up to ∼60 km/h were recorded, however most ladybirds were found between ∼150 and 500 m, and had a mean displacement of 30 km/h. Average flight time was estimated, using tethered flight experiments, to be 36.5 minutes, but flights of up to two hours were observed. Ladybirds are therefore potentially able to travel 18 km in a "typical" high-altitude flight, but up to 120 km if flying at higher altitudes, indicating a high capacity for long-distance dispersal. There were strong seasonal trends in ladybird abundance, with peaks corresponding to the highest temperatures of mid-summer, and warm air temperature was the key driver of ladybird flight. Climatic warming may therefore increase the potential for long-distance dispersal in these species. Low aphid abundance was a second significant factor, highlighting the important role of aphid population dynamics in ladybird dispersal. This research illustrates the utility of radar for studying high-altitude insect flight and has important implications for predicting long-distance dispersal.

A physical explanation of the temperature dependence of physiological processes mediated by cilia and flagella.

The majority of biological rates are known to exhibit temperature dependence. Here I reveal a direct link between temperature and ecologically relevant rates such as swimming speeds in Archaea, Bacteria, and Eukaryotes as well as fluid-pumping and filtration rates in many metazoans, and show that this relationship is driven by movement rates of cilia and flagella. I develop models of the temperature dependence of cilial and flagellar movement rates and evaluate these with an extensive compilation of data from the literature. The model captures the temperature dependence of viscosity and provides a mechanistic and biologically interpretable explanation for the temperature dependence of a range of ecologically relevant processes; it also reveals a clear dependence on both reaction rate-like processes and the physics of the environment. The incorporation of viscosity allows further insight into the effects of environmental temperature variation and of processes, such as disease, that affect the viscosity of blood or other body fluids.

Effect of particulate contamination on adhesive ability and repellence in two species of ant (Hymenoptera; Formicidae).

Tarsal adhesive pads are crucial for the ability of insects to traverse their natural environment. Previous studies have demonstrated that for both hairy and smooth adhesive pads, significant reduction in adhesion can occur because of contamination of these pads by wax crystals present on plant surfaces or synthetic microspheres. In this paper, we focus on the smooth adhesive pads of ants and study systematically how particulate contamination and the subsequent loss of adhesion depends on particle size, particle surface energy, humidity and species size. To this end, workers of ant species Polyrhachis dives and Myrmica scabrinodis (Hymenoptera; Formicidae) were presented with loose synthetic powder barriers with a range of powder diameters (1-500 µm) and surface energies (PTFE or glass), which they would have to cross in order to escape the experimental arena. The barrier experiments were conducted for a range of humidities (10-70%). Experimental results and scanning electron microscopy confirm that particulate powders adversely affect the adhesive ability of both species of ant on smooth substrates via contamination of the arolia. Specifically, the loss of adhesion was found to depend strongly on particle diameter, but only weakly on particle type, with the greatest loss occurring for particle diameters smaller than the claw dimensions of each species, and no effect of humidity was found. We also observed that ants were repelled by the powder barriers which led to a decrease of adhesion prior to their eventual crossing, suggesting that insect antennae may play a role in probing the mechanical fragility of substrates before crossing them.

Comparative analysis of teleost genome sequences reveals an ancient intron size expansion in the zebrafish lineage.

We have developed a bioinformatics pipeline for the comparative evolutionary analysis of Ensembl genomes and have used it to analyze the introns of the five available teleost fish genomes. We show our pipeline to be a powerful tool for revealing variation between genomes that may otherwise be overlooked with simple summary statistics. We identify that the zebrafish, Danio rerio, has an unusual distribution of intron sizes, with a greater number of larger introns in general and a notable peak in the frequency of introns of approximately 500 to 2,000 bp compared with the monotonically decreasing frequency distributions of the other fish. We determine that 47% of D. rerio introns are composed of repetitive sequences, although the remainder, over 331 Mb, is not. Because repetitive elements may be the origin of the majority of all noncoding DNA, it is likely that the remaining D. rerio intronic sequence has an ancient repetitive origin and has since accumulated so many mutations that it can no longer be recognized as such. To study such an ancient expansion of repeats in the Danio, lineage will require further comparative analysis of fish genomes incorporating a broader distribution of teleost lineages.

Mechanisms of temperature-dependent swimming: the importance of physics, physiology and body size in determining protist swimming speed.

Body temperatures and thus physiological rates of poikilothermic organisms are determined by environmental temperature. The power an organism has available for swimming is largely dependent on physiological rates and thus body temperature. However, retarding forces such as drag are contingent on the temperature-dependent physical properties of water and on an organism's size. Consequently, the swimming ability of poikilotherms is highly temperature dependent. The importance of the temperature-dependent physical properties of water (e.g. viscosity) in determining swimming speed is poorly understood. Here we propose a semi-mechanistic model to describe how biological rates, size and the physics of the environment contribute to the temperature dependency of microbial swimming speed. Data on the swimming speed and size of a predatory protist and its protist prey were collected and used to test our model. Data were collected by manipulating both the temperature and the viscosity (independently of temperature) of the organism's environment. Protists were either cultured in their test environment (for several generations) or rapidly exposed to their test environment to assess their ability to adapt or acclimate to treatments. Both biological rates and the physics of the environment were predicted to and observed to contribute to the swimming speed of protists. Body size was not temperature dependent, and protists expressed some ability to acclimate to changes in either temperature or viscosity. Overall, using our parameter estimates and novel model, we are able to suggest that 30 to 40% (depending on species) of the response in swimming speed associated with a reduction in temperature from 20 to 5°C is due to viscosity. Because encounter rates between protist predators and their prey are determined by swimming speed, temperature- and viscosity-dependent swimming speeds are likely to result in temperature- and viscosity-dependent trophic interactions.

Variability in isotope discrimination factors in coral reef fishes: implications for diet and food web reconstruction.

Interpretation of stable isotope ratios of carbon and nitrogen (δ(13)C and δ(15)N) is generally based on the assumption that with each trophic level there is a constant enrichment in the heavier isotope, leading to diet-tissue discrimination factors of 3.4‰ for (15)N (ΔN) and ∼0.5‰ for (13)C (ΔC). Diet-tissue discrimination factors determined from paired tissue and gut samples taken from 152 individuals from 26 fish species at Ningaloo Reef, Western Australia demonstrate a large amount of variability around constant values. While caution is necessary in using gut contents to represent diet due to the potential for high temporal variability, there were significant effects of trophic position and season that may also lead to variability in ΔN under natural conditions. Nitrogen enrichment increased significantly at higher trophic levels (higher tissue δ(15)N), with significantly higher ΔN in carnivorous species. Changes in diet led to significant changes in ΔN, but not tissue δ(15)N, between seasons for several species: Acanthurus triostegus, Chromis viridis, Parupeneus signatus and Pomacentrus moluccensis. These results confirm that the use of meta-analysis averages for ΔN is likely to be inappropriate for accurately determining diets and trophic relationships using tissue stable isotope ratios. Where feasible, discrimination factors should be directly quantified for each species and trophic link in question, acknowledging the potential for significant variation away from meta-analysis averages and, perhaps, controlled laboratory diets and conditions.

Direct and indirect effects of temperature on the population dynamics and ecosystem functioning of aquatic microbial ecosystems.

1. While much is known about the direct effect that temperature can have on aquatic communities, less is known about its indirect effect via the temperature dependence of viscosity and temperature-dependent trophic interactions. 2. We manipulated the temperature (5-20 °C) and the viscosity (equivalent to 5-20 °C) of water in laboratory-based bacteria-protist communities. Communities contained food chains with one, two or three trophic levels. Responses measured were population dynamics (consumer carrying capacity and growth rate, average species population density, and the coefficient of variation of population density through time) and ecosystem function (decomposition). 3. Temperature, viscosity and food chain length produced significant responses in population dynamics. Temperature-dependent viscosity had a significant effect on the carrying capacity and growth rates of consumers, as well as the average density of the top predator. Overall, indirect effects of temperature via changes in viscosity were subtle in comparison to the indirect effect of temperature via trophic interactions. 4. Our results highlight the importance of direct and indirect effects of temperature, mediated through trophic interactions and physical changes in the environment, both for population dynamics and ecosystem processes. Future mechanistic modelling of effects of environmental change on species will benefit from distinguishing the different mechanisms of the overall effect of temperature.