Reproductive biotechnologies for endangered mammalian species

Assisted reproductive techniques (gamete cryopreservation, artificial insemination, embryo transfer, and in vitro fertilization) allow to propagate small fragmented populations of wild endangered species or domestic breeds. There are the best way for producing several offspring from selected genitors in order to avoid inbreeding depression. However, few mammalian species have been well studied for their reproductive biology whereas huge differences have been observed between these species. Furthermore, materials, methods and experimental designs have to be adapted for each case and each limiting factor (wildness, poor quantity of biological material, disparate locations). Genome resource banking is currently arising and the most applied reproductive biotechnology remains artificial insemination. Assisted reproductive techniques currently developed in domestic species (intracytoplasmic sperm injection, nuclear transfer) may offer new opportunities for the propagation of endangered species.     

A review on reproductive biotechnologies for conservation of endangered mammalian species

This review describes the use of modern reproductive biotechnologies or assisted reproductive techniques (ART) including artificial insemination, embryo transfer/sexing, in vitro fertilization, gamete/embryo micromanipulation, semen sexing, genome resource banking, and somatic cell nuclear transfer (cloning) in conservation programs for endangered mammalian species. Such biotechnologies allow more offspring to be obtained from selected parents to ensure genetic diversity and may reduce the interval between generations. However, the application of reproductive biotechnologies for endangered free-living mammals is rarer than for endangered domestic breeds. Progress in ART for non-domestic species will continue at a slow pace due to limited resources, but also because the management and conservation of endangered species is biologically quite complex. In practice, current reproductive biotechnologies are species-specific or inefficient for many endangered animals because of insufficient knowledge on basic reproduction like estrous cycle, seasonality, structural anatomy, gamete physiology and site for semen deposition or embryo transfer of non-domestic species.     

Animal board invited review: Germplasm technologies for use with poultry

Over the last century, several reproductive biotechnologies beyond the artificial incubation of eggs were developed to improve poultry breeding stocks and conserve their genetic diversity. These include artificial insemination (AI), semen storage, diploid primordial germ cell (PGC) methodologies, and gonad tissue storage and transplantation. Currently, AI is widely used for selection purposes in the poultry industry, in the breeding of turkeys and guinea fowl, and to solve fertility problems in duck interspecies crosses for the production of mule ducklings. The decline in some wild game species has also raised interest in reproductive technologies as a means of increasing the production of fertile eggs, and ultimately the number of birds that can be raised. AI requires viable sperm to be preserved in vitro for either short (fresh) or longer periods (chilling or freezing). Since spermatozoa are the most easily accessed sex cells, they are the cell type most commonly preserved by genetic resource banks. However, the cryopreservation of sperm only preserves half of the genome, and it cannot preserve the W chromosome. For avian species, the problem of preserving oocytes and zygotes may be solved via the cryopreservation and transplantation of PGCs and gonad tissue. The present review describes all these procedures and discusses how combining these different technologies allows poultry populations to be conserved and even rapidly reconstituted.     

Pregnancies following long luteal phases in southern white rhinoceros (Ceratotherium simum simum)

All extant species in the Rhinocerotidae family are experiencing escalating threats in the wild, making self-sustaining captive populations essential genetic reservoirs for species survival. Assisted reproductive technologies (ARTs) will become increasingly important for achieving and maintaining ex situ population sustainability and genetic diversity. Previous reports have shown that a large proportion of captive southern white rhinoceros (SWR) females are irregularly cyclic or acyclic, and that cycling females display two different estrous cycle lengths of approximately 30 or 70 days. It has been suggested that the longer estrous cycle length is infertile or subfertile, as no term pregnancies have been observed following long cycles. Here we report the achievement of two pregnancies following long luteal phases, using ovulation induction and artificial insemination with either fresh or frozen-thawed semen. One female SWR conceived on the first insemination attempt and gave birth to a live offspring. A second female conceived twice in consecutive long cycles although the first embryo was resorbed by 33 days post-insemination. A pregnancy from this female's second insemination is ongoing with expected parturition in November 2019. Whether prolonged estrous cycles in SWR are subfertile or infertile in natural breeding situations remains unclear. However, our findings demonstrate that the application of ARTs following prolonged cycles can result the successful establishment of pregnancies in SWR. Therefore, with ARTs, female SWR otherwise considered nonreproductive due to long estrous cycles may still have the potential for representation and contribution to the ex situ population.     

Sperm cryopreservation in wild animals

Extinction of a species represents the loss of a resource evolved through eons of mutations and natural selection. Reproductive technologies, including artificial insemination, embryo transfer, in vitro fertilization, gamete/embryo micromanipulation, semen sexing, and genome resource banking (GRB) have all been developed with the aim of solving existing problems and preserving genetic material for conservation purposes. Although protocols from domestic or non-threatened related species have been extrapolated to nondomestic and endangered species, usually these reproductive technologies are species-specific and inefficient in many nondomestic species because of insufficient knowledge on their basic reproduction biology and the need for species-specific customization. Since spermatozoa are usually more accessible and come in large numbers compared to oocytes and embryos, they are considered the primary cell type preserved in most emerging GRBs. For this purpose, semen from endangered species is currently cryopreserved to avail long-term storage. Due to the intractability of most exotic species, semen collection without chemical restraint is limited to only a handful of species and individuals. Viable epididymal spermatozoa can be obtained from dead or castrated animals, but this resource is limited. Electroejaculation, artificial vagina, abdominal massage, and/or transrectal, ultrasound-guided, massage of the accessory sex glands of living animals are viable alternative methods of semen collection. The ultimate goal is to adapt and optimize collection and cryopreservation protocols for each species, making it feasible, among other things, to collect gametes in the wild and introduce them into captive or isolated populations to increase genetic diversity. Recent advances in these fields have allowed the establishment of GRBs for many threatened species.     

Ultrasonography as an important tool for the development and application of reproductive technologies in non-domestic species

Ultrasound imaging in reproductive sciences offers new opportunities regarding optimization of the induction of the sexual cycle and ovulation, superovulation regimes, contraception programs, semen collection and testicular sperm extraction techniques, ovum pick up and ovarian transplantation procedures, as well as the application of artificial insemination, embryo collection and transfer. In non-domestic species, most of which lack basic data, ultrasonography is an ideal tool to study reproductive biology in both captive and wild populations. The use of this imaging modality led us to develop new, or modify established, reproductive technologies. Ultrasonography has been an integral part of over 200 assisted reproduction procedures in 17 mammalian species performed by our research team between 1992 and 1999. These procedures included the initial characterization of sexual cycles, hormonal cycle induction, semen collection by electroejaculation or manual stimulation, non-surgical artificial insemination (AI), non-surgical embryo transfer and temporary hormonal contraception. For these investigations, a variety of newly developed equipment was applied and species-specific hormonal treatments designed. We used several commercial and customized ultrasound systems with a variety of technical features. Some relevant improvements of these applications will be described and the role of ultrasonography elucidated to.     

Genomics of brown algae: current advances and future prospects

The analysis of the complete genome sequence of the filamentous brown alga Ectocarpus provided many new insights into brown algal biology and has improved our understanding of how this organism has adapted to its seashore environment. Since the publication of the genome sequence in 2010, numerous studies have continued the analysis of the constituent genes or have combined genome data with experimental work, allowing progress in several key areas, including metabolism and reproductive biology. Ectocarpus will continue to be exploited as a model organism in future years, but genomic approaches should also be extended to additional brown algal species in order to fully exploit the diversity of this phylogenetic group and to facilitate the application of new knowledge to economically important seaweeds such as kelps.     

Female reproductive cycles of wild female felids

Many felid species are endangered because of destructive human activities. As a result, zoos are being tasked with sustaining genetically healthy populations in case of catastrophic extinctions. Unfortunately, with the exception of a few species, most felids do not reproduce well in captivity. The ability to track reproductive activity via hormones is key to developing successful ex situ breeding programs. Through the development of noninvasive fecal hormone monitoring techniques, a high degree of variability in estrous cycle characteristics has been found to exist across the taxon, including the type of ovulation. For example, although all felids have induced ovulations, the occurrence of spontaneous ovulations varies across species, and even between individuals within a species. Clouded leopards, fishing cats and margays frequently have spontaneous ovulations, whereas these are rarely observed in the cheetah, tigrina and ocelot. There are marked species differences in the impact of season on reproductive function, with some being exquisitely sensitive to photoperiod (e.g., Pallas' cat), some moderately affected (tiger, clouded leopard, snow leopard), and others that are not influenced at all (e.g., ocelot, tigrina, margay, lion, leopard, fishing cat). One of the greatest challenges remaining is overcoming the problems associated with highly variable ovarian responses to ovulation induction therapies used with assisted reproductive procedures, like artificial insemination (AI). Success is relatively high in the cheetah and ocelot, but few pregnancies have resulted after AI in clouded leopard, fishing cat and tiger. Current knowledge of the reproductive physiology of nondomestic felids, including aspects of the anatomy, behavior and ovarian cycles will be presented, and how the rapidly growing endocrine database is aiding ex situ management efforts.     

Artificial insemination in marsupials

Assisted breeding technology (ART), including artificial insemination (AI), has the potential to advance the conservation and welfare of marsupials. Many of the challenges facing AI and ART for marsupials are shared with other wild species. However, the marsupial mode of reproduction and development also poses unique challenges and opportunities. For the vast majority of marsupials, there is a dearth of knowledge regarding basic reproductive biology to guide an AI strategy. For threatened or endangered species, only the most basic reproductive information is available in most cases, if at all. Artificial insemination has been used to produce viable young in two marsupial species, the koala and tammar wallaby. However, in these species the timing of ovulation can be predicted with considerably more confidence than in any other marsupial. In a limited number of other marsupials, such precise timing of ovulation has only been achieved using hormonal treatment leading to conception but not live young. A unique marsupial ART strategy which has been shown to have promise is cross-fostering; the transfer of pouch young of a threatened species to the pouches of foster mothers of a common related species as a means to increase productivity. For the foreseeable future, except for a few highly iconic or well studied species, there is unlikely to be sufficient reproductive information on which to base AI. However, if more generic approaches can be developed; such as ICSI (to generate embryos) and female synchronization (to provide oocyte donors or embryo recipients), then the prospects for broader application of AI/ART to marsupials are promising.     

Genetic passportization and identification of Siberian cranes (Grus leucogeranus Pallas) in captivity

The genetic diversity of the founders of an artificial population of the Siberian crane Grus leucogeranus Pallas (rare species of cranes) was characterized using 10 microsatellite loci. It was established that the allelic diversity (on average, 5.9 alleles per locus) and genic (H _O = 0.739) diversity of the Siberian crane is rather high and comparable with the estimations for natural populations of different crane species. Genetic passportization of the birds (119 individuals) from the register of the Siberian crane International Studbook was carried out at the initial stage. The efficiency of genetic passportization for individual identification, identification of the origin, paternity analysis, and exclusion of inbreeding was demonstrated in Siberian cranes under natural mating and artificial insemination. Cases of natural reproduction in pairs of Siberian cranes imprinted to the human and continuous storage of spermatozoa in the female reproductive ducts were registered.     

The importance and potential of artificial insemination in CANDES (companion animals, non-domestic, endangered species)

Artificial insemination (AI) is the least invasive assisted reproductive technology, and is therefore of great interest to breeders of companion animals, non-domestic, and endangered species (CANDES). This most fundamental artificial breeding technique circumvents physical or behavioral impediments to natural mating and provides the means for genetic exchange between populations without transfer of live animals. In addition, because oocytes grow, mature and are fertilized in vivo and embryos are not subjected to in vitro culture conditions, AI eliminates the epigenetic effects on the female gamete that are inherent in more invasive assisted reproductive technologies. Although the management of CANDES differs significantly from current livestock husbandry practices, the cattle industry is a powerful example of the potential for AI to enhance the genetic health and sustainability of animal populations. Ultimately, successful AI requires sperm of adequate quality and quantity, oocytes that have attained nuclear maturation and cytoplasmic competence, operational gamete transport systems, accurate timing, and proper placement of sperm in the female reproductive tract. Increased understanding of semen collection, evaluation and preservation techniques, estrus synchronization and superovulation, estrus and ovulation detection, and insemination instrumentation is needed for each CANDES before AI success rates will approach those of the livestock industry. Concentrated, collaborative research in these areas must be encouraged among private breeders, universities and zoological institutions to realize the full potential of AI in the management of CANDES.     

Genetic markers for stallion fertility--lessons from humans and mice

Our knowledge on the many aspects of mammalian reproduction in general and equine reproduction in particular has greatly increased during the last 15 years. Advances in the understanding of the physiology, cell biology, and biochemistry of reproduction have facilitated genetic analyses of fertility. Currently, there are more than 200 genes known that are involved in the production of fertile sperm cells. The completion of a number of mammalian genome projects will aid in the investigation of these genes in different species. Great progress has been made in the understanding of genetic aberrations that lead to male infertility. Additionally, the first genetic mechanisms are being discovered that contribute to the quantitative variation of fertility traits in fertile male animals. As artificial insemination (AI) represents a widespread technology in horse breeding, semen quality traits may eventually become an additional selection criterion for breeding stallions. Current research activities try to identify genetic markers that correlate to these semen quality traits. Here, we will review the current state of genetic research in male fertility and offer some perspectives for future research in horses.     

A genome‐wide scan for selection signatures in Nellore cattle

Brazilian Nellore cattle (Bos indicus) have been selected for growth traits for over more than four decades. In recent years, reproductive and meat quality traits have become more important because of increasing consumption, exports and consumer demand. The identification of genome regions altered by artificial selection can potentially permit a better understanding of the biology of specific phenotypes that are useful for the development of tools designed to increase selection efficiency. Therefore, the aims of this study were to detect evidence of recent selection signatures in Nellore cattle using extended haplotype homozygosity methodology and BovineHD marker genotypes (>777 000 single nucleotide polymorphisms) as well as to identify corresponding genes underlying these signals. Thirty‐one significant regions (P < 0.0001) of possible recent selection signatures were detected, and 19 of these overlapped quantitative trait loci related to reproductive traits, growth, feed efficiency, meat quality, fatty acid profiles and immunity. In addition, 545 genes were identified in regions harboring selection signatures. Within this group, 58 genes were associated with growth, muscle and adipose tissue metabolism, reproductive traits or the immune system. Using relative extended haplotype homozygosity to analyze high‐density single nucleotide polymorphism marker data allowed for the identification of regions potentially under artificial selection pressure in the Nellore genome, which might be used to better understand autozygosity and the effects of selection on the Nellore genome.     

Observing copepods through a genomic lens

Background

Copepods outnumber every other multicellular animal group. They are critical components of the world's freshwater and marine ecosystems, sensitive indicators of local and global climate change, key ecosystem service providers, parasites and predators of economically important aquatic animals and potential vectors of waterborne disease. Copepods sustain the world fisheries that nourish and support human populations. Although genomic tools have transformed many areas of biological and biomedical research, their power to elucidate aspects of the biology, behavior and ecology of copepods has only recently begun to be exploited.

Discussion

The extraordinary biological and ecological diversity of the subclass Copepoda provides both unique advantages for addressing key problems in aquatic systems and formidable challenges for developing a focused genomics strategy. This article provides an overview of genomic studies of copepods and discusses strategies for using genomics tools to address key questions at levels extending from individuals to ecosystems. Genomics can, for instance, help to decipher patterns of genome evolution such as those that occur during transitions from free living to symbiotic and parasitic lifestyles and can assist in the identification of genetic mechanisms and accompanying physiological changes associated with adaptation to new or physiologically challenging environments. The adaptive significance of the diversity in genome size and unique mechanisms of genome reorganization during development could similarly be explored. Genome-wide and EST studies of parasitic copepods of salmon and large EST studies of selected free-living copepods have demonstrated the potential utility of modern genomics approaches for the study of copepods and have generated resources such as EST libraries, shotgun genome sequences, BAC libraries, genome maps and inbred lines that will be invaluable in assisting further efforts to provide genomics tools for copepods.

Summary

Genomics research on copepods is needed to extend our exploration and characterization of their fundamental biological traits, so that we can better understand how copepods function and interact in diverse environments. Availability of large scale genomics resources will also open doors to a wide range of systems biology type studies that view the organism as the fundamental system in which to address key questions in ecology and evolution.     

Assisted reproductive technologies in captive rhinoceroses

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