Annual Review of Animal Biosciences - Volume 10, 2022

Procedures to maintain viability of mammalian gametes and embryos in vitro, including cryopreservation, have been exceedingly valuable for my research over the past 55 years. Keeping sperm viable in vitro enables artificial insemination, which, when combined with selective breeding, often is the most effective approach to making rapid genetic change in a population. Superovulation and embryo transfer constitute a parallel approach for amplifying reproduction of female mammals. More recent developments include sexing of semen, in vitro fertilization, cloning by nuclear transfer, and genetic modification of germline cells, tools that are enabled by artificial insemination and/or embryo transfer for implementation. I have been fortunate in being able to contribute to the development of many of the above techniques, and to use them for research and applications for improving animal agriculture. Others have built on this work to circumvent human infertility, assist reproduction of companion animals, and rescue endangered species. It also has been a privilege to teach, mentor, and be mentored in this area. Resulting worldwide friendships have enriched me personally and professionally.

Tardigrades are ubiquitous meiofauna that are especially renowned for their exceptional extremotolerance to various adverse environments, including pressure, temperature, and even ionizing radiation. This is achieved through a reversible halt of metabolism triggered by desiccation, a phenomenon called anhydrobiosis. Recent establishment of genome resources for two tardigrades, Hypsibius exemplaris and Ramazzottius varieornatus, accelerated research to uncover the molecular mechanisms behind anhydrobiosis, leading to the discovery of many tardigrade-unique proteins. This review focuses on the history, methods, discoveries, and current state and challenges regarding tardigrade genomics, with an emphasis on molecular anhydrobiology. Remaining questions and future perspectives regarding prospective approaches to fully elucidate the molecular machinery of this complex phenomenon are discussed.

Antarctic notothenioid fishes are the classic example of vertebrate adaptive radiation in a marine environment. Notothenioids diversified from a single common ancestor ∼22 Mya to between 120 and 140 species today, and they represent ∼90% of fish biomass on the continental shelf of Antarctica. As they diversified in the cold Southern Ocean, notothenioids evolved numerous traits, including osteopenia, anemia, cardiomegaly, dyslipidemia, and aglomerular kidneys, that are beneficial or tolerated in their environment but are pathological in humans. Thus, notothenioids are models for understanding adaptive radiations, physiological and biochemical adaptations to extreme environments, and genetic mechanisms of human disease. Since 2014, 16 notothenioid genomes have been published, which enable a first-pass holistic analysis of the notothenioid radiation and the genetic underpinnings of novel notothenioid traits. Here, we review the notothenioid radiation from a genomic perspective and integrate our insights with recent observations from other fish radiations.

Toxin evolution in animals is one of the most fascinating and complex subjects of scientific inquiry today. Gaining an understanding of toxins poses a multifaceted challenge given the diverse modes of acquisition, evolutionary adaptations, and abiotic components that affect toxin phenotypes. Here, we highlight some of the main genetic and ecological factors that influence toxin evolution and discuss the role of antagonistic interactions and coevolutionary dynamics in shaping the direction and extent of toxicity and resistance in animals. We focus on toxic Pacific newts (family Salamandridae, genus Taricha) as a system to investigate and better evaluate the widely distributed toxin they possess, tetrodotoxin (TTX), and the hypothesized model of arms-race coevolution with snake predators that is used to explain phenotypic patterns of newt toxicity. Finally, we propose an alternative coevolutionary model that incorporates TTX-producing bacteria and draws from an elicitor–receptor concept to explain TTX evolution and ecology.

Repeatedly and recently evolved sympatric morphs exhibiting consistent phenotypic differences provide natural experimental replicates of speciation. Because such morphs are observed frequently in Salmonidae, this clade provides a rare opportunity to uncover the genomic mechanisms underpinning speciation. Such insight is also critical for conserving salmonid diversity, the loss of which could have significant ecological and economic consequences. Our review suggests that genetic differentiation among sympatric morphs is largely nonparallel apart from a few key genes that may be critical for consistently driving morph differentiation. We discuss alternative levels of parallelism likely underlying consistent morph differentiation and identify several factors that may temper this incipient speciation between sympatric morphs, including glacial history and contemporary selective pressures. Our synthesis demonstrates that salmonids are useful for studying speciation and poses additional research questions to be answered by future study of this family.

During the teleost radiation, extensive development of the direct innervation mode of hypothalamo-pituitary communication was accompanied by loss of the median eminence typical of mammals. Cells secreting follicle-stimulating hormone and luteinizing hormone cells are directly innervated, distinct populations in the anterior pituitary. So far, ∼20 stimulatory and ∼10 inhibitory neuropeptides, 3 amines, and 3 amino acid neurotransmitters are implicated in the control of reproduction. Positive and negative sex steroid feedback loops operate in both sexes. Gene mutation models in zebrafish and medaka now challenge our general understanding of vertebrate neuropeptidergic control. New reproductive neuropeptides are emerging. These include but are not limited to nesfatin 1, neurokinin B, and the secretoneurins. A generalized model for the neuroendocrine control of reproduction is proposed. Hopefully, this will serve as a research framework on diverse species to help explain the evolution of neuroendocrine control and lead to the discovery of new hormones with novel applications.

Thoroughbred horses have been selected for racing performance for more than 400 years. Despite continued selection, race times have not improved significantly during the past 60 years, raising the question of whether genetic variation for racing performance still exists. Studies using phenotypes such as race time, money earned, and handicapping, however, demonstrate that there is extensive variation within these traits and that they are heritable. Even so, these are poor measures of racing success since Thoroughbreds race at different ages and distances and on different types of tracks, and some may not race at all. With the advent of genomic tools, DNA variants are being identified that contribute to racing success. Aside from strong associations for myostatin variants with best racing distance, weak to modest associations with racing phenotypes are reported for other genomic regions. These data suggest that diverse genetic strategies have contributed to producing a successful racehorse, and genetic variation contributing to athleticism remains important.

Microbial communities associated with deep-sea animals are critical to the establishment of novel biological communities in unusual environments. Over the past few decades, rapid exploration of the deep sea has enabled the discovery of novel microbial communities, some of which form symbiotic relationships with animal hosts. Symbiosis in the deep sea changes host physiology, behavior, ecology, and evolution over time and space. Symbiont diversity within a host is often aligned with diverse metabolic pathways that broaden the environmental niche for the animal host. In this review, we focus on microbiomes and obligate symbionts found in different deep-sea habitats and how they facilitate survival of the organisms that live in these environments. In addition, we discuss factors that govern microbiome diversity, host specificity, and biogeography in the deep sea. Finally, we highlight the current limitations of microbiome research and draw a road map for future directions to advance our knowledge of microbiomes in the deep sea.

Animal microbiomes are occasionally considered as an extension of host anatomy, physiology, and even their genomic architecture. Their compositions encompass variable and constant portions when examined across multiple hosts. The latter, termed the core microbiome, is viewed as more accommodated to its host environment and suggested to benefit host fitness. Nevertheless, discrepancies in its definitions, characteristics, and importance to its hosts exist across studies. We survey studies that characterize the core microbiome, detail its current definitions and available methods to identify it, and emphasize the crucial need to upgrade and standardize the methodologies among studies. We highlight ruminants as a case study and discussthe link between the core microbiome and host physiology and genetics, as well as potential factors that shape it. We conclude with main directives of action to better understand the host–core microbiome axis and acquire the necessary insights into its controlled modulation.

Animals harbor diverse communities of microbes within their gastrointestinal tracts. Phylogenetic relationship, diet, gut morphology, host physiology, and ecology all influence microbiome composition within and between animal clades. Emerging evidence points to host genetics as also playing a role in determining gut microbial composition within species. Here, we discuss recent advances in the study of microbiome heritability across a variety of animal species. Candidate gene and discovery-based studies in humans, mice, Drosophila, Caenorhabditis elegans, cattle, swine, poultry, and baboons reveal trends in the types of microbes that are heritable and the host genes and pathways involved in shaping the microbiome. Heritable gut microbes within a host species tend to be phylogenetically restricted. Host genetic variation in immune- and growth-related genes drives the abundances of these heritable bacteria within the gut. With only a small slice of the metazoan branch of the tree of life explored to date, this is an area rife with opportunities to shed light into the mechanisms governing host–microbe relationships.

Demand for ruminant products (dairy products, beef, and sheep meat) is increasing rapidly with population and income growth and the acceleration of urbanization. However, ruminant animals exert the highest environmental impacts and consume the most resources in the livestock system. Increasing studies have focused on various measures to reduce ammonia, greenhouse gas emissions, and resource depletion from ruminant production to consumption. This review offers supply- and demand-side management strategies to reduce the environmental impact of ruminant products and emphasizes the mitigation potential of coupling livestock production with cultivation and renewable energy. On a global scale, more attention should be paid to the green-source trade and to strengthening global technology sharing. The success of these strategies depends on the cost effectiveness of technology, public policy, and financial support. Future studies and practice should focus on global database development for sharing mitigation strategies, thus facilitating technology innovations and socioeconomic feasibility.

The lack of preclinical models of spontaneous ovarian cancer (OVCA), a fatal gynecological malignancy, is a significant barrier to generating information on early changes indicative of OVCA. In contrast to rodents, laying hens develop OVCA spontaneously, with remarkable similarities to OVCA in women regarding tumor histology, OVCA dissemination, immune responses, and risk factors. These important features of OVCA will be useful to develop an early detection test for OVCA, which would significantly reduce mortality rates; preventive strategies; immunotherapeutics; prevention of resistance to chemotherapeutics; and exploration of gene therapies. A transvaginal ultrasound (TVUS) imaging method for imaging of hen ovarian tumors has been developed. Hens can be monitored prospectively by using serum markers, together with TVUS imaging, to detect early-stage OVCA, provided that a panel of serum markers can be established and imaging agents developed. Recent sequencing of the chicken genome will further facilitate the hen model to explore gene therapies against OVCA.

Analogies between placentation, in particular the behavior of trophoblast cells, and cancer have been noted since the beginning of the twentieth century. To what degree these can be explained as a consequence of the evolution of placentation has been unclear. In this review, we conclude that many similarities between trophoblast and cancer cells are shared with other, phylogenetically older processes than placentation. The best candidates for cancer hallmarks that can be explained by the evolution of eutherian placenta are mechanisms of immune evasion. Another dimension of the maternal accommodation of the placenta with an impact on cancer malignancy is the evolution of endometrial invasibility. Species with lower degrees of placental invasion tend to have lower vulnerability to cancer malignancy. We finally identify several areas in which one could expect to see coevolutionary changes in placental and cancer biology but that, to our knowledge, have not been explored.

Considerable progress has been made with the development of culture systems for the in vitro growth and maturation (IVGM) of oocytes from the earliest-staged primordial follicles and from the more advanced secondary follicles in rodents, ruminants, nonhuman primates, and humans. Successful oocyte production in vitro depends on the development of a dynamic culture strategy that replicates the follicular microenvironment required for oocyte activation and to support oocyte growth and maturation in vivo while enabling the coordinated and timely acquisition of oocyte developmental competence. Significant heterogeneity exists between the culture protocols used for different stages of follicle development and for different species. To date, the fertile potential of IVGM oocytes derived from primordial follicles has been realized only in mice. Although many technical challenges remain, significant advances have been made, and there is an increasing consensus that complete IVGM will require a dynamic, multiphase culture approach. The production of healthy offspring from in vitro–produced oocytes in a secondary large animal species is a vital next step before IVGM can be tested for therapeutic use in humans.

Bluetongue virus (BTV) is an arthropod-borne, segmented double-stranded RNA virus that can cause severe disease in both wild and domestic ruminants. BTV evolves via several key mechanisms, including the accumulation of mutations over time and the reassortment of genome segments.Additionally, BTV must maintain fitness in two disparate hosts, the insect vector and the ruminant. The specific features of viral adaptation in each host that permit host-switching are poorly characterized. Limited field studies and experimental work have alluded to the presence of these phenomena at work, but our understanding of the factors that drive or constrain BTV's genetic diversification remains incomplete. Current research leveraging novel approaches and whole genome sequencing applications promises to improve our understanding of BTV's evolution, ultimately contributing to the development of better predictive models and management strategies to reduce future impacts of bluetongue epizootics.

Chagas disease, a neglected tropical disease present in the Americas, is caused by the parasite Trypanosoma cruzi and is transmitted by triatomine kissing bug vectors. Hundreds of vertebrate host species are involved in the ecology of Chagas disease. The sylvatic nature of most triatomines found in the United States accounts for high levels of animal infections but few reports of human infections. This review focuses on triatomine distributions and animal infections in the southern United States. A quantitative synthesis of available US data from triatomine bloodmeal analysis studies shows that dogs, humans, and rodents are key taxa for feeding triatomines. Imperfect and unvalidated diagnostic tools for wildlife complicate the study of animal T. cruzi infections, and integrated vector management approaches are needed to reduce parasite transmission in nature. The diversity of animal species involved in Chagas disease ecology underscores the importance of a One Health approach for disease research and management.

T cells are an essential component of the adaptive immune system. Over the last 15 years, a constantly growing toolbox with which to study T cell biology in pigs has allowed detailed investigations on these cells in various viral and bacterial infections. This review provides an overview on porcine CD4, CD8, and γδ T cells and the current knowledge on the differentiation of these cells following antigen encounter. Where available, the responses of these cells to viral infections like porcine reproductive and respiratory syndrome virus, classical swine fever virus, swine influenza A virus, and African swine fever virus are outlined. In addition, knowledge on the porcine T cell response to bacterial infections like Actinobacillus pleuropneumoniae and Salmonella Typhimurium is reviewed. For CD4 T cells, the response to the outlined infections is reflected toward the Th1/Th2/Th17/Tfh/Treg paradigm for functional differentiation.

An estimated 1.3 million Salmonella infections and 420 deaths occur annually in the United States, with an estimated economic burden of $3.7 billion. More than 50% of US swine operations test positive for Salmonella according to the National Animal Health Monitoring System, and 20% of Salmonella from swine are multidrug resistant (resistant to ≥3 antimicrobial classes) as reported by the National Antimicrobial Resistance Monitoring System. This review on Salmonella in swine addresses the current status of these topics by discussing antimicrobial resistance and metal tolerance in Salmonella and the contribution of horizontal gene transfer. A major challenge in controlling Salmonella is that Salmonella is a foodborne pathogen in humans but is often a commensal in food animals and thereby establishes an asymptomatic reservoir state in such animals, including swine. As food animal production systems continue to expand and antimicrobial usage becomes more limited, the need for Salmonella interventions has intensified. A promising mitigation strategy is vaccination against Salmonella in swine to limit animal, environmental, and food contamination.

As medical and pharmacological technology advances, new and complex modalities of disease treatment that are more personalized and targeted are being developed. Often these modalities must be validated in the presence of critical components of the human biological system. Given the incongruencies between murine and human biology, as well as the human-tropism of certain drugs and pathogens, the selection of animal models that accurately recapitulate the intricacies of the human biological system becomes more salient for disease modeling and preclinical testing. Immunodeficient mice engrafted with functional human tissues (so-called humanized mice), which allow for the study of physiologically relevant disease mechanisms, have thus become an integral aspect of biomedical research. This review discusses the recent advancements and applications of humanized mouse models on human immune system and liver humanization in modeling human diseases, as well as how they can facilitate translational medicine.