Annual Review of Animal Biosciences - Volume 5, 2017

This article is a combination of an autobiography and a review of outstanding research done by over 70 graduate students, postdoctoral fellows, and visiting scientists along with excellent collaborators during my over-40-year career as a professor of reproductive physiology at the University of Illinois, Urbana-Champaign. I have also shared thoughts on mentoring, how research has changed over the years, and the future of reproductive physiology. I provide the reader with a snapshot of the challenges faced by a woman eager to obtain a PhD under the guidance of renowned professors in the early 1970s and to be hired as the first woman, and the only permanent female faculty member, for more than 20 years on a faculty of 40 men. As a comparative reproductive physiologist, I describe the various animal models used because they were the best models to answer specific questions in reproduction. Also, my graduate students and postdoctoral fellows were given the freedom to identify their research topics, articulate hypotheses to be tested, and select appropriate animal models. This approach caused students to take ownership of their research, resulting in the development of independent and creative scientists and over 170 publications, excluding chapters in top-tier journals. Finally, I am so grateful for a truly rich life mentoring graduate students and postdoctoral fellows who have become my lifelong friends.

Campylobacter includes a group of genetically diverse species causing a range of diseases in animals and humans. The bacterium is frequently associated with two economically important and epidemiologically distinct reproductive diseases in ruminants: enzootic infectious infertility in cattle owing to Campylobacter fetus subsp. venerealis and abortions in sheep, goats, and cattle. Septic abortion, usually epizootic in sheep, has been historically associated with C. fetus subsp. fetus and to a lesser extent with Campylobacter jejuni. However, there has been a dramatic species shift in the etiology of Campylobacter abortions in recent years: C. jejuni has now replaced C. fetus subsp. fetus as the predominant cause of sheep abortion in the United States, which appears to be driven primarily by clonal expansion of a hypervirulent tetracycline-resistant C. jejuni clone. Here we provide a review on the recent advances in understanding the pathobiology of Campylobacter infections in animals, with an emphasis on the diseases in ruminants, covering epidemiology, pathogenesis, genomics, and control measures.

For the important foodborne pathogen Salmonella enterica to cause disease or persist in pigs, it has evolved an intricate set of interactions between itself, the host, and the indigenous microflora of the host. S. enterica must evade the host's immune system and must also overcome colonization resistance mediated by the pig's indigenous microflora. The inflammatory response against S. enterica provides the bacteria with unique metabolites and is thus exploited by S. enterica for competitive advantage. During infection, changes in the composition of the indigenous microflora occur that have been associated with a breakdown in colonization resistance. Healthy pigs that are low-level shedders of S. enterica also exhibit alterations in their indigenous microflora similar to those in ill animals. Here we review the literature on the interactions that occur between swine, S. enterica, and the indigenous microflora and discuss methods to reduce or prevent colonization of pigs with S. enterica.

This article summarizes the relevant definitions related to biomarkers; reviews the general processes related to biomarker discovery and ultimate acceptance and use; and finally summarizes and reviews, to the extent possible, examples of the types of biomarkers used in animal species within veterinary clinical practice and human and veterinary drug development. We highlight opportunities for collaboration and coordination of research within the veterinary community and leveraging of resources from human medicine to support biomarker discovery and validation efforts for veterinary medicine.

Vaccination is essential in livestock farming and in companion animal ownership. Nucleic acid vaccines based on DNA or RNA provide an elegant alternative to those classical veterinary vaccines that have performed suboptimally. Recent advances in terms of rational design, safety, and efficacy have strengthened the position of nucleic acid vaccines in veterinary vaccinology. The present review focuses on replicon vaccines designed for veterinary use. Replicon vaccines are self-amplifying viral RNA sequences that, in addition to the sequence encoding the antigen of interest, contain all elements necessary for RNA replication. Vaccination results in high levels of in situ antigen expression and induction of potent immune responses. Both positive- and negative-stranded viruses have been used to construct replicons, and they can be delivered as RNA, DNA, or viral replicon particles. An introduction to the biology and the construction of different viral replicon vectors is given, and examples of veterinary replicon vaccine applications are discussed.

Adequate protein intake is critical for health and development. Generally, protein of animal origin is of higher quality for humans owing to its amino acid pattern and good digestibility. When administered in mixtures it can enhance the quality of plant proteins, but its availability is often low in low-income communities, especially in young children, the elderly, and pregnant and lactating women, who have increased requirements and in whom high-quality protein also stimulates (bone) growth and maintenance. Although high protein intake was associated with increased type 2 diabetes mellitus risk, milk and seafood are good sources of branched chain amino acids and taurine, which act beneficially on glucose metabolism and blood pressure. However, high consumption of protein-rich animal food is also associated with adverse health effects and higher risk for noncommunicable diseases, partly related to other components of these foods, like saturated fatty acids and potential carcinogens in processed meat but also the atherogenic methionine metabolite homocysteine. In moderation, however, animal proteins are especially important for health maintenance in vulnerable persons.

There is sustained growth in the number of tropical cattle, which represent more than half of all cattle worldwide. By and large, most research in tropical areas is still focused on breeds of cattle, their particular advantages or disadvantages in tropical areas, and the tropical forages or feeds that could be usefully fed to them. A consistent issue for adaptation to climate is the heat of tropical environments. Changing the external characteristics of the animal, such as color and coat characteristics, is one way to adapt, and there are several major genes for these traits. However, further improvement in heat tolerance and other adaptation traits will need to use the entire genome and all physical and physiological systems. Apart from the response to heat, climate forcing through methane emission identifies dry season weight loss as an important if somewhat neglected trait in climate adaptation of cattle. The use of genome-estimated breeding values in tropical areas is in its infancy and will be difficult to implement, but will be essential for rapid, coordinated genetic improvement. The difficulty of implementation cannot be exaggerated and may require major improvements in methodology.

Among the components of the female reproductive tract, the ovarian pool of follicles and their enclosed oocytes are highly sensitive to hyperthermia. Heat-induced alterations in small antral follicles can be expressed later as compromised maturation and developmental capacity of the ovulating oocyte. This review summarizes the most up-to-date information on the effects of heat stress on the oocyte with an emphasis on unclear points and open questions, some of which might involve new research directions, for instance, whether preantral follicles are heat resistant. The review focuses on the follicle-enclosed oocytes, provides new insights into the cellular and molecular responses of the oocyte to elevated temperature, points out the role of the follicle microenvironment, and discusses some mechanisms that might underlie oocyte impairment. Mechanisms include nuclear and cytoplasmic maturation, mitochondrial function, apoptotic pathways, and oxidative stress. Understanding the mechanism by which heat stress compromises fertility might enable development of new strategies to mitigate its effects.

Animal production in China has achieved considerable progress and contributes to 46% of the total agriculture output value of the country. However, this fast expansion of animal production has led to environmental pollution. In this article, we review the status of soil, water, and air pollution associated with animal production in China and analyze the main sources of the pollutants. The government has promulgated regulations and standards, and effective models and technologies have been developed to control pollution during the last 10 years. Because nutrition and feed strategies represent the most effective method of controlling environmental pollution at the source, this review focuses on nutritional technologies, including accurate feed formulation, rational use of additives, and proper processing of feeds. The advances of modern biotechnology and big data systems also provide more modern approaches to decreasing wastage release. These nutritional strategies are expected to promote sustainable development of animal production.

The teleost fish embryo is particularly sensitive to petroleum hydrocarbons (polycyclic aromatic hydrocarbons, PAHs) at two distinct stages of development. The first is early during cleavage stages when PAHs alter normal signaling associated with establishment of the dorsal-ventral axis. This disruption involves the Wnt/β-catenin pathway and results in hyperdorsalized embryos that do not survive to hatching. The second, more sensitive period is during heart development, when oil and PAHs cause abnormal development of the heart as well as cardiac edema and arrhythmia. Even at extremely low levels (ng/L), PAHs cause subtle edema and altered contractility and heart rate, which impair swimming performance. Some PAHs are extremely phototoxic, such that exposures to trace concentrations result in severe membrane damage and mortality in sunlight. The developing fish embryo is a sensitive indicator of petroleum constituents in the environment, and healthy populations of fish likely require limited PAH exposure during development.

In mammalian species, endometrial receptivity is driven by maternal factors independently of embryo signals. When pregnancy initiates, paracrine secretions of the preattachment embryo are essential both for maternal recognition and endometrium preparation for implantation and for coordinating development of embryonic and extraembryonic tissues of the conceptus. This review mainly focuses on domestic large animal species. We first illustrate the major steps of preattachment embryo development, including elongation in bovine, ovine, porcine, and equine species. We next highlight conceptus secretions that are involved in the communication between extraembryonic and embryonic tissues, as well as between the conceptus and the endometrium. Finally, we introduce experimental data demonstrating the intimate connection between conceptus secretions and endometrial activity and how adverse events perturbing this interplay may affect the progression of implantation that will subsequently impact pregnancy outcome, postnatal health, and expression of production traits in livestock offspring.

One of the grand challenges facing our society today is finding solutions for feeding the world sustainably. The food-versus-fuel debate is a controversy embedded in this challenge, involving the trade-offs of using grains and oilseeds for biofuels production versus animal feed and human food. However, only 6% of total global grain produced is used to produce ethanol. Furthermore, biofuels coproducts contribute to sustainability of food production because only 1% to 2.5% of the overall energy efficiency is lost from converting crops into biofuels and animal feed, and approximately one-third of the corn used to produce ethanol is recovered as feed coproducts. Extensive research has been conducted over the past 15 years on biofuels coproducts to (a) optimize their use for improving caloric and nutritional efficiency in animal feeds, (b) identify benefits and limitations of use in various animal diets, (c) characterize their unique nutraceutical properties, and (d) evaluate their environmental impacts.

We describe the domestication of the species, explore its value to agriculture and bioscience, and compare its immunoglobulin (Ig) genes to those of other vertebrates. For encyclopedic information, we cite earlier reviews and chapters. We provide current gene maps for the heavy and light chain loci and describe their polygeny and polymorphy. B-cell and antibody repertoire development is a major focus, and we present findings that challenge several mouse-centric paradigms. We focus special attention on the role of ileal Peyer's patches, the largest secondary lymphoid tissues in newborn piglets and a feature of all artiodactyls. We believe swine fetal development and early class switch evolved to provide natural secretory IgA antibodies able to prevent translocation of bacteria from the gut while the bacterial PAMPs drive development of adaptive immunity. We discuss the value of using the isolator piglet model to address these issues.

Understanding the timing and geographic context of dog origins is a crucial component for understanding human history, as well as the evolutionary context in which the morphological and behavioral divergence of dogs from wolves occurred. A substantial challenge to understanding domestication is that dogs have experienced a complicated demographic history. An initial severe bottleneck was associated with domestication followed by postdivergence gene flow between dogs and wolves, as well as population expansions, contractions, and replacements. In addition, because the domestication of dogs occurred in the relatively recent past, much of the observed polymorphism may be shared between dogs and wolves, limiting the power to distinguish between alternative models of dog history. Greater insight into the domestication process will require explicit tests of alternative models of domestication through the joint analysis of whole genomes from modern lineages and ancient wolves and dogs from across Eurasia.

Genomic selection has revolutionized dairy cattle breeding. Since 2000, assays have been developed to genotype large numbers of single-nucleotide polymorphisms (SNPs) at relatively low cost. The first commercial SNP genotyping chip was released with a set of 54,001 SNPs in December 2007. Over 15,000 genotypes were used to determine which SNPs should be used in genomic evaluation of US dairy cattle. Official USDA genomic evaluations were first released in January 2009 for Holsteins and Jerseys, in August 2009 for Brown Swiss, in April 2013 for Ayrshires, and in April 2016 for Guernseys. Producers have accepted genomic evaluations as accurate indications of a bull's eventual daughter-based evaluation. The integration of DNA marker technology and genomics into the traditional evaluation system has doubled the rate of genetic progress for traits of economic importance, decreased generation interval, increased selection accuracy, reduced previous costs of progeny testing, and allowed identification of recessive lethals.

During the last decade, ancient DNA research has been revolutionized by the availability of increasingly powerful DNA sequencing and ancillary genomics technologies, giving rise to the new field of paleogenomics. In this review, we show how our understanding of the genetic basis of animal domestication and the origins and dispersal of livestock and companion animals during the Upper Paleolithic and Neolithic periods is being rapidly transformed through new scientific knowledge generated with paleogenomic methods. These techniques have been particularly informative in revealing high-resolution patterns of artificial and natural selection and evidence for significant admixture between early domestic animal populations and their wild congeners.

Pheromones were identified as chemical signals used for intraspecific communication in insects (e.g., sexual attraction) in the 1950s. However, only almost 40 years later the vomeronasal receptors type-1 (V1R) and type-2 (V2R) were identified, usually associated with the presence of a vomeronasal organ (VNO). VRs are widespread in amphibians, reptiles, and mammals, but birds lost the VNO. Similarly, fishes lack VRs and a VNO but can still detect pheromones, instead using the olfactory receptors related to class A and class C G protein–coupled receptors. Here, we review recent evidence on VR repertoire contraction/expansion in vertebrates. We assess the association between VNO development and VR repertoire size. Phylogenetic relationships and selective pressures illuminate the dynamic evolutionary history of the VRs in vertebrates.

Animal models offer heuristic research tools to understand the causes of human diseases and to identify potential treatments. With rapidly evolving genetic engineering technologies, mutations identified in a human disorder can be generated in the mouse genome. Phenotypic outcomes of the mutation are then explicated to confirm hypotheses about causes and to discover effective therapeutics. Most neurodevelopmental, neurodegenerative, and psychiatric disorders are diagnosed primarily by their prominent behavioral symptoms. Mouse behavioral assays analogous to the human symptoms have been developed to analyze the consequences of mutations and to evaluate proposed therapeutics preclinically. Here we describe the range of mouse behavioral tests available in the established behavioral neuroscience literature, along with examples of their translational applications. Concepts presented have been successfully used in other species, including flies, worms, fish, rats, pigs, and nonhuman primates. Identical strategies can be employed to test hypotheses about environmental causes and gene × environment interactions.