Animal Life History Research Articles

Early and later life environmental enrichment affect specific antibody responses and blood leukocyte subpopulations in pigs

This study addressed the impact of early and later life environmental enrichment, and their combination, on specific antibody responses and peripheral blood leukocyte subpopulations in pigs. Pigs were kept in either barren (B1) or enriched (E1) housing from birth, and half of the pigs switched to barren or enriched housing on day 47, resulting in four treatment combinations: B1B2, B1E2, E1B2, E1E2). Pigs were immunized with keyhole limpet hemocyanin-conjugated trinitrophenyl (KLH-TNP) on day 74 and 109 to induce primary and secondary antibody responses. Blood samples were taken weekly until day 130, and IgM and IgG antibody responses were measured. Leukocyte subpopulations were measured on day 74 and 130. Time course of the antibody responses was not affected by housing. Early life enrichment increased the IgG response to KLH, particularly the primary one. At day 74 the relative frequency of lymphocytes, DC and SLA-II expression on monocytes were higher in E1 pigs, whereas the percentage of granulocytes tended to be lower in E1 pigs at day 74. Early life enrichment increased the SLA-II expression on monocytes, the granulocyte to lymphocyte ratio, and tended to increase the percentage of granulocytes, but tended to decrease the percentage of monocytes at day 130. Later life enrichment reduced percentages of CD4+CD8α+ T cells before and after immunization and the SLA-II expression on monocytes at day 74, the percentage of granulocytes and the granulocyte to lymphocyte ratio at day 130. Notably, early and later life housing interacted in their effects on several immune parameters. KLH-IgM responses (both primary and secondary) were affected by the interaction between early and later life housing. IgM titers were higher for B1B2 than for E1E2, with the switched animals (B1E2 and E1B2) moving towards the titers of the animals kept in their later life environment from birth onwards. At day 130 the percentage of gamma delta T cells, CD8α+ cytotoxic T cells and DC were not different between pigs kept in B1B2 and E1E2, but there was a clear impact of the switch in housing conditions, particularly for the pigs that changed from barren to enriched housing. We also found effects of coping style (personality) and sex on some immune parameters. In conclusion, both early life and later life enrichment, and, notably a switch in housing conditions influenced specific antibodies and leukocyte subpopulations in pigs. The current study implies that the early life history of animals and the (mis)match with their current environment could thus be of major importance for their immune system. Further research is needed to investigate potential consequences for the pigs’ health.

External environment and internal state in relation to life-history behavioural profiles of adolescents in nine countries.

The external environment has traditionally been considered as the primary driver of animal life history (LH). Recent research suggests that animals' internal state is also involved, especially in forming LH behavioural phenotypes. The present study investigated how these two factors interact in formulating LH in humans. Based on a longitudinal sample of 1223 adolescents in nine countries, the results show that harsh and unpredictable environments and adverse internal states in childhood are each uniquely associated with fast LH behavioural profiles consisting of aggression, impulsivity, and risk-taking in adolescence. The external environment and internal state each strengthened the LH association of the other, but overall the external environment was more predictive of LH than was the internal state. These findings suggest that individuals rely on a multitude and consistency of sensory information in more decisively calibrating LH and behavioural strategies.

Toward a metabolic theory of life history

The life histories of animals reflect the allocation of metabolic energy to traits that determine fitness and the pace of living. Here, we extend metabolic theories to address how demography and mass-energy balance constrain allocation of biomass to survival, growth, and reproduction over a life cycle of one generation. We first present data for diverse kinds of animals showing empirical patterns of variation in life-history traits. These patterns are predicted by theory that highlights the effects of 2 fundamental biophysical constraints: demography on number and mortality of offspring; and mass-energy balance on allocation of energy to growth and reproduction. These constraints impose 2 fundamental trade-offs on allocation of assimilated biomass energy to production: between number and size of offspring, and between parental investment and offspring growth. Evolution has generated enormous diversity of body sizes, morphologies, physiologies, ecologies, and life histories across the millions of animal, plant, and microbe species, yet simple rules specified by general equations highlight the underlying unity of life.

Visual Opsin Diversity in Sharks and Rays.

The diversity of color vision systems found in extant vertebrates suggests that different evolutionary selection pressures have driven specializations in photoreceptor complement and visual pigment spectral tuning appropriate for an animal's behavior, habitat, and life history. Aquatic vertebrates in particular show high variability in chromatic vision and have become important models for understanding the role of color vision in prey detection, predator avoidance, and social interactions. In this study, we examined the capacity for chromatic vision in elasmobranch fishes, a group that have received relatively little attention to date. We used microspectrophotometry to measure the spectral absorbance of the visual pigments in the outer segments of individual photoreceptors from several ray and shark species, and we sequenced the opsin mRNAs obtained from the retinas of the same species, as well as from additional elasmobranch species. We reveal the phylogenetically widespread occurrence of dichromatic color vision in rays based on two cone opsins, RH2 and LWS. We also confirm that all shark species studied to date appear to be cone monochromats but report that in different species the single cone opsin may be of either the LWS or the RH2 class. From this, we infer that cone monochromacy in sharks has evolved independently on multiple occasions. Together with earlier discoveries in secondarily aquatic marine mammals, this suggests that cone-based color vision may be of little use for large marine predators, such as sharks, pinnipeds, and cetaceans.

Negative allometric growth during ontogeny in the large pelagic filter-feeding basking shark

Many pelagic shark species change body and fin shape isometrically or by positive allometry during ontogeny. But some large apex predators such as the white shark Carcharodon carcharias or the tiger shark Galeocerdo cuvier show distinct negative allometry, especially in traits related to feeding (head) or propulsion (caudal fin). In particular, changes in propulsion are attributed to a shift in swimming mode. The more heterocercal caudal fin of younger individuals with its large caudal fin span seemingly aids in hunting small, agile prey. In contrast, the less heterocercal caudal fin with a larger fin area in larger individuals aids a long-distance slow swimming mode. We were interested if negative allometric effects can be observed in a planktivorous shark, the basking shark Cetorhinus maximus, a large species adapted to long-distance slow swimming. To address this question, we compared three size classes, specifically < 260 cm (juveniles), 299–490 cm (subadults), and from adults > 541 cm total length. Comparing literature data, we found negative allometric growth of the head and of the caudal fin, but a more rapid decrease of relative caudal fin size than of relative head length. Hereby, we provide the first evidence for early negative allometric growth of the caudal fin in a large pelagic filter-feeding shark. Our study further demonstrates that ecomorphological approaches may add valuable insight into the life history of animals that are challenging to study in their natural habitat, including large roving sharks such as the basking shark.

Speed consensus and the ‘Goldilocks principle’ in flocking birds (Columba livia)

The evolution of group living transformed the history of animal life on earth, yielding substantial selective benefits. Yet, without overcoming fundamental challenges such as how to coordinate movements with conspecifics, animals cannot maintain cohesion, and coordination is thus a prerequisite for the evolution of sociality in nonstationary animals. Although it has been considered that animal groups must coordinate the timing and direction of movements, coordinating speed is also essential to prevent the group from splitting. We investigated speed consensus in homing pigeon, Columba livia, flocks using high-resolution GPS. Despite observable differences in average solo speed (which was positively correlated with bird mass) compromises of up to 6% from the preferred solo speed were made to reach consensus in flocks. These results match theory which suggests that groups fly at an intermediate of solo speeds, which suggests speed averaging. By virtue of minimizing extreme compromises, speed averaging can maximize selective benefits across the group, suggesting shared consensus for group speed could be ubiquitous across taxa. Nevertheless, despite group-wide advantages, contemporary flight models have suggested unequal energetic costs in favour of individuals with intermediate body mass/preferred speed (hence the ‘Goldilocks principle’).

One Hundred Pressing Questions on the Future of Global Fish Migration Science, Conservation, and Policy

Migration is a widespread but highly diverse component of many animal life histories. Fish migrate throughout the world’s oceans, within lakes and rivers, and between the two realms, transporting matter, energy, and other species (e.g. microbes) across boundaries. Migration is therefore a process responsible for myriad ecosystem services. Many human populations depend on the presence of predictable migrations of fish for their subsistence and livelihoods. Although much research has focused on fish migration, many questions remain in our rapidly changing world. We assembled a diverse team of fundamental and applied scientists who study fish migrations in marine and freshwater environments to identify pressing unanswered questions. Our exercise revealed questions within themes related to understanding the migrating individual’s internal state, navigational mechanisms, locomotor capabilities, external drivers of migration, the threats confronting migratory fish including climate change, and the role of migration. In addition, we identified key requirements for aquatic animal management, restoration, policy, and governance. Lessons revealed included the difficulties in generalizing among species and populations, and in understanding the levels of connectivity facilitated by migrating fishes. We conclude by identifying priority research needed for assuring a sustainable future for migratory fishes.

First person – Vishwanath Varma

ABSTRACTFirst Person is a series of interviews with the first authors of a selection of papers published in Biology Open, helping early-career researchers promote themselves alongside their papers. Vishwanath Varma is first author on ‘Accuracy of fruit-fly eclosion rhythms evolves by strengthening circadian gating rather than developmental fine-tuning’, published in BiO. Vishwanath conducted the research described in this article while a PhD student in Prof. Vijay Kumar Sharma's lab at the Jawaharlal Nehru Centre for Advanced Scientific Research, India. He is now a postdoctoral fellow in the lab of Dr V. V. Binoy at the National Institute of Advanced Studies, India, investigating the links between animal behavior, physiology and life history, and how they adapt to changing ecological conditions.

Animal life history is shaped by the pace of life and the distribution of age-specific mortality and reproduction.

Animals exhibit an extraordinary diversity of life history strategies. These realized combinations of survival, development and reproduction are predicted to be constrained by physiological limitations and by trade-offs in resource allocation. However, our understanding of these patterns is restricted to a few taxonomic groups. Using demographic data from 121 species, ranging from humans to sponges, we test whether such trade-offs universally shape animal life history strategies. We show that, after accounting for body mass and phylogenetic relatedness, 71% of the variation in animal life history strategies can be explained by life history traits associated with the fast-slow continuum (pace of life) and with a second axis defined by the distribution of age-specific mortality hazards and the spread of reproduction. While we found that life history strategies are associated with metabolic rate and ecological modes of life, surprisingly similar life history strategies can be found across the phylogenetic and physiological diversity of animals.

Designing network‐connected systems for ecological research and education

AbstractWhile networked sensors are becoming a ubiquitous part of many human lives, their applications to the study of wild animals have been largely limited to off‐the‐shelf and stand‐alone technologies such as web cameras. However, purpose‐designed systems, applying features found in Internet‐of‐Things devices, enable more efficient gathering, managing, and disseminating of a diverse array of data needed to study the life histories of wild animals. We illustrate these claims based on our development of a system of networked nest boxes that we created to study nesting birds in urban environments. This system uses general‐purpose processors within nest boxes to perform edge computing to control data acquisition, processing, and management from multiple sensors. A central data‐management system permits easy access to all data, once downloaded, which has facilitated our uses to date of this system for formal university‐ and school‐level education, and informal science education.

Possible links between extreme oxygen perturbations and the Cambrian radiation of animals.

The role of oxygen as a driver for early animal evolution is widely debated. During the Cambrian explosion, episodic radiations of major animal phyla occurred coincident with repeated carbon isotope fluctuations. However, the driver of these isotope fluctuations and potential links to environmental oxygenation are unclear. Here, we report high-resolution carbon and sulphur isotope data for marine carbonates from the southeastern Siberian Platform that document the canonical explosive phase of the Cambrian radiation from ~524 to ~514 Myr ago. These analyses demonstrate a strong positive covariation between carbonate δ13C and carbonate-associated sulphate δ34S through five isotope cycles. Biogeochemical modelling suggests that this isotopic coupling reflects periodic oscillations in atmospheric O2 and the extent of shallow ocean oxygenation. Episodic maxima in the biodiversity of animal phyla directly coincided with these extreme oxygen perturbations. Conversely, the subsequent Botoman–Toyonian animal extinction events (~514 to ~512 Myr ago) coincided with decoupled isotope records that suggest a shrinking marine sulphate reservoir and expanded shallow marine anoxia. We suggest that fluctuations in oxygen availability in the shallow marine realm exerted a primary control on the timing and tempo of biodiversity radiations at a crucial phase in the early history of animal life

Selection for longer lived sperm within ejaculate reduces reproductive ageing in offspring.

Males produce numerous sperm in a single ejaculate that greatly outnumber their potential egg targets. Recent studies found that phenotypic and genotypic variation among sperm in a single ejaculate of a male affects the fitness and performance of the resulting offspring. Specifically, within‐ejaculate sperm selection for sperm longevity increased the performance of the resulting offspring in several key life‐history traits in early life. Because increased early‐life reproductive performance often correlates with rapid ageing, it is possible that within‐ejaculate sperm selection increases early‐life fitness at the cost of accelerated senescence. Alternatively, within‐ejaculate sperm selection could improve offspring quality throughout the life cycle, including reduced age‐specific deterioration. We tested the two alternative hypotheses in an experimental setup using zebrafish Danio rerio. We found that within‐ejaculate sperm selection for sperm longevity reduced age‐specific deterioration of fecundity and offspring survival but had no effect on fertilization success in males. Remarkably, we found an opposing effect of within‐ejaculate sperm selection on female fecundity, where selection for sperm longevity resulted in increased early‐life performance followed by a slow decline, while females sired by unselected sperm started low but increased their fecundity with age. Intriguingly, within‐ejaculate sperm selection also reduced the age‐specific decline in fertilization success in females, suggesting that selection for sperm longevity improves at least some aspects of female reproductive ageing. These results demonstrate that within‐ejaculate variation in sperm phenotype contributes to individual variation in animal life histories in the two sexes and may have important implications for assisted fertilization programs in livestock and humans.

Immune trade‐offs shape disease outcomes at individual and population scales

Most aspects of an animal's life history are subject to trade‐offs, where a beneficial change in one trait is linked to a detrimental change in another. Immune function is no different and trade‐offs between different components of the immune system are well described. Importantly, these trade‐offs may have significant implications for infectious disease outcomes. For example, trade‐offs in immunity may be particularly important during concurrent infection (i.e. co‐infection), if the host immune response to one pathogen negatively affects the response to another. Focusing on trade‐offs between the T helper cell 1 (Th1) and Th2 branches of the immune system, we examined how infection with gastrointestinal worms, which trigger a Th2‐type immune response in the host, affects the immune response to a bacterial pathogen (Mycobacterium bovis, causative agent of bovine tuberculosis) for which a Th1‐type response is required for defense. By integrating experimental and longitudinal studies of a wild population of African buffalo (Syncerus caffer), we show that this well‐known trade‐off in immune function operates on both ecological and evolutionary time scales with repercussions for individual disease severity and population‐level disease dynamics.Support or Funding InformationNational Science Foundation (Award #DEB‐1102493)This abstract is from the Experimental Biology 2019 Meeting. There is no full text article associated with this abstract published in The FASEB Journal.

Jointly estimating survival and mortality: integrating recapture and recovery data from complex multiple predator systems

Identifying where, when, and how many animals live and die over time is principal to understanding factors that influence population dynamics. Capture–recapture–recovery (CRR) models are widely used to estimate animal survival and, in many cases, quantify specific causes of mortality (e.g., harvest, predation, starvation). However, the restrictive CRR framework can inhibit the consideration and inclusion of some types of recovery data. We developed an extension to the CRR framework to allow for the incorporation of recoveries from indeterminate temporal or spatial origin. This model jointly estimates cause-specific mortality and survival probabilities across multiple spatial and temporal scales, while accounting for differences in mortality-specific reporting and recovery rates. We fitted the model to data on a group of juvenile steelhead trout (Oncorhynchus mykiss) marked with passive integrated transponder tags in the Columbia River basin, USA. Following tagging and release, fish were detected alive at up to six downstream locations and/or recovered dead on one of nine bird colonies during seaward migration. We estimated that, in aggregate, avian predators consumed 31% of juvenile steelhead during outmigration to the ocean (95% CRI: [27, 36]). Colony-specific predation rates ranged from 95% of all steelhead mortality within some reaches. This integrated modelling approach provides a flexible framework to integrate multiple recapture and recovery data sources, providing a more holistic understanding of animal life history, including direct comparisons of cause-specific mortality factors and the cumulative impact of multiple mortality factors across time or space.

Toads phenotypically adjust their chemical defences to anthropogenic habitat change

Despite the well-documented effects of human-induced environmental changes on the morphology, physiology, behaviour and life history of wild animals, next to nothing is known about how anthropogenic habitats influence anti-predatory chemical defence, a crucial fitness component of many species. We investigated the amount and composition of defensive toxins in adult common toads (Bufo bufo) captured in natural, agricultural and urban habitats, and in their offspring raised in a common-garden experiment. We found that, compared to toads captured from natural habitats, adults from both types of anthropogenic habitats had larger toxin glands (parotoids) and their toxin secretion contained higher concentrations of bufagenins, the more potent class of bufadienolide toxins. Furthermore, urban toads had lower concentrations of bufotoxins, the compounds with lower toxicity. None of these differences were present in the captive-raised juveniles; instead, toadlets originating from agricultural habitats had smaller parotoids and lower bufotoxin concentrations. These results suggest that toads’ chemical defences respond to the challenges of anthropogenic environments via phenotypic plasticity. These responses may constitute non-adaptive consequences of pollution by endocrine-disrupting chemicals as well as adaptive adjustments to the altered predator assemblages of urban and agricultural habitats.

Improved camouflage through ontogenetic colour change confers reduced detection risk in shore crabs.

Animals from many taxa, from snakes and crabs to caterpillars and lobsters, change appearance with age, but the reasons why this occurs are rarely tested.We show the importance that ontogenetic changes in coloration have on the camouflage of the green shore crabs (Carcinus maenas), known for their remarkable phenotypic variation and plasticity in colour and pattern.In controlled conditions, we reared juvenile crabs of two shades, pale or dark, on two background types simulating different habitats for 10 weeks.In contrast to expectations for reversible colour change, crabs did not tune their background match to specific microhabitats, but instead, and regardless of treatment, all developed a uniform dark green phenotype. This parallels changes in shore crab appearance with age observed in the field.Next, we undertook a citizen science experiment at the Natural History Museum London, where human subjects (“predators”) searched for crabs representing natural colour variation from different habitats, simulating predator vision.In concert, crabs were not hardest to find against their original habitat, but instead, the dark green phenotype was hardest to detect against all backgrounds.The evolution of camouflage can be better understood by acknowledging that the optimal phenotype to hide from predators may change over the life history of many animals, including the utilization of a generalist camouflage strategy. A plain language summary is available for this article.

Larval nutritional mode and swimming behaviour in ciliated marine larvae

AbstractSwimming propagules (embryos and larvae) are a critical component of the life histories of benthic marine animals. Larvae that feed (planktotrophic) have been assumed to swim faster, disperse farther and have more complex behavioural patterns than non-feeding (lecithotrophic) larvae. However, a number of recent studies challenge these early assumptions, suggesting a need to revisit them more formally. The current review presents a quantitative analysis of swimming speed and body size in planktotrophic and lecithotrophic propagules across five major marine phyla (Porifera, Cnidaria, Annelida, Mollusca and Echinodermata). Results of the comparative study showed that swimming speed differences among ciliated propagules can be driven by taxonomy, adult mobility (motile vs sessile) and/or larval nutritional mode. On a phylogenetic level, distinct patterns emerge across phyla and life stages, whereby planktotrophic propagules swim faster in some of them, and lecithotrophic propagules swim faster in others. Interestingly, adults with sessile and sedentary lifestyles produce propagules that swam faster than the propagules produced by motile adults. Understanding similarities and differences among marine propagules associated with different reproductive strategies and adult lifestyles are significant from ecological, evolutionary and applied perspectives. Patterns of swimming can directly impact the dispersal/recruitment potential with incidence on the design of larval rearing methods and marine protected areas.

Ontogeny and phylogeny of the mammalian chondrocranium: the cupula nasi anterior and associated structures of the anterior head region

BackgroundThe study of chondrocrania has a long tradition with a focus on single specimens and stages. It revealed great interspecific diversity and a notion of intraspecific variation. As an embryonic structure, the chondrocranium is subject to major changes in ontogeny with resorption and ossification of different cartilaginous structures. The cupula nasi anterior is the anteriormost portion of the cartilaginous nasal capsule and is expected to mirror much of the animal's life history and lifestyle. Its diversity in mammals is reflected in the external nasal anatomy of newborns. Marsupials and placentals show marked differences, likely related to breathing and suckling behavior.ResultsWe examined histological sections of five marsupial and three placentals species and traced the development of the cupula nasi anterior and the anterior nasal capsule. We found ontogenetic variation for nearly 50% of the 43 characters defined herein. By comparing to the literature and considering ontogenetic variation, we performed an analysis of character evolution in 70 mammalian species and reconstructed the nasal anatomy of the therian ancestor.ConclusionsAt birth, marsupials have a complete but simple cupula nasi anterior, whereas placentals display a more diverse morphology due to reductions and variations of chondrocranial elements. The more compact nasal capsule in marsupials is related to a long and strong fixation to the mother’s teat after birth. Within marsupials and placentals, several derived characters distinguish major taxa, probably related to developmental and functional constraints. The reconstructed ancestral anatomy of the cupula nasi anterior supports the hypothesis that the therian ancestor was placental-like and that the marsupial lifestyle is more derived.

From texts to teeth: A multi-isotope study of sheep and goat herding practices in the Late Bronze Age (‘Mycenaean’) polity of Knossos, Crete

Linear B administrative documents of the late second millennium BC from urban Knossos, Crete, reveal that spatially extensive and centrally monitored sheep flocks and wool production played a fundamental role in Mycenaean palatial economy. Here we employ multi-isotope (δ13C, δ18O, 87Sr/86Sr) analysis of sequentially sampled sheep and goat tooth enamel bioapatite to explore life histories of animals consumed at Knossos. Interpretation of isotopic results incorporates new baseline data on 87Sr/86Sr ratios of bioavailable Sr from modern Cretan plants collected in relevant zones. Results reveal a variety of herding regimes, including seasonal (‘wet/winter’ to ‘dry/summer’) vertical movement of sheep from lowland to highland locations, more restricted mobility for goats in lowland to mid-altitude territories, possible input of fodder to goat diet, and exploitation of a range of plant ecosystems. Results broadly match documentary evidence and ethnographic/ecological expectations for sheep and goat herding at varying scales and underline the role of Knossos in mobilising resources from a range of herding systems and territories.

The Mitochondrial Contribution to Animal Performance, Adaptation, and Life-History Variation.

Animals display tremendous variation in their rates of growth, reproductive output, and longevity. While the physiological and molecular mechanisms that underlie this variation remain poorly understood, the performance of the mitochondrion has emerged as a key player. Mitochondria not only impact the performance of eukaryotes via their capacity to produce ATP, but they also play a role in producing heat and reactive oxygen species and function as a major signaling hub for the cell. The papers included in this special issue emerged from a symposium titled "Inside the Black Box: The Mitochondrial Basis of Life-history Variation and Animal Performance." Based on studies of diverse animal taxa, three distinct themes emerged from these papers. (1) When linking mitochondrial function to components of fitness, it is crucial that mitochondrial assays are performed in conditions as close as the intracellular conditions experienced by the mitochondria in vivo. (2) Functional plasticity allows mitochondria to retain their performance, as well as that of their host, over a range of exogenous conditions, and selection on mitochondrial and nuclear-derived proteins can optimize the match between the environment and the bioenergetic capacity of the mitochondrion. Finally, (3) studies of wild and wild-derived animals suggest that mitochondria play a central role in animal performance and life history strategy. Taken as a whole, we hope that these papers will foster discussion and inspire new hypotheses and innovations that will further our understanding of the mitochondrial processes that underlie variation in life history traits and animal performance.