Abstract
In brief
Current research on the genomics, ecology and reproductive biology of hystricomorph rodents relies on the pioneering studies of B J Weir and I W Rowlands. We show the enduring influence of a symposium on hystricomorph biology held 50 years ago.
Abstract
The rodent suborder Hystricomorpha comprises seven families from Africa and Asia and ten from South America, where they have undergone an extensive radiation and occupy a variety of biomes. Although the guinea pig was a common laboratory rodent, little was known about reproductive biology in the other species until the ambitious research programme of Barbara Weir and her mentor I W Rowlands. Much of their work and of others then in the field was summarized at a symposium held 50 years ago at The Zoological Society of London. Currently, there is a resurgence of interest in the reproductive biology of the South American species. Compared to other rodents, unique features include a long gestation, a long oestrous cycle, a tendency to form accessory corpora lutea and a vaginal closure membrane. There is a distinctive placental structure, the subplacenta. Most give birth to precocial young. Individual species exhibit peculiarities such as polyovulation, systematic fetal loss and an active female prostate. Here, we highlight the achievements of Barbara Weir and show how her legacy has been sustained in the twenty-first century by South American scientists.
Introduction
Hystricomorph rodents reached South America in the Eocene and underwent an extensive radiation. They occupy many different habitats: there are terrestrial, arboreal, scansorial, fossorial, semi-fossorial and semiaquatic species (Upham & Patterson 2015). The guinea pig (Cavia porcellus) was domesticated as a food source and subsequently adopted as a laboratory animal (Endersby 2007, Lord et al. 2020). However, little was known about the biology of other hystricomorphs until the seminal studies of Barbara Weir at the Wellcome Institute of Comparative Physiology of the Zoological Society of London (ZSL). She had moved there when her supervisor I W Rowlands was appointed Director, taking with him the chinchilla colony that had been established at Cambridge by A S Parkes FRS (1900–1990) (Polge 2006). A few additional species were available from London Zoo but usually as post-mortem specimens. Barbara Weir went about establishing husbandry practices for several hystricomorphs and established breeding colonies with animals she had collected on two field expeditions to Argentina.
This research programme culminated 50 years ago with a symposium held in 1973 at the ZSL and published the following year (Rowlands & Weir 1974). In the meantime, Weir had made a career transition. Rowlands retired in 1974 and was replaced by Robert D Martin, a primatologist. The hystricomorph breeding colonies were moved to Cambridge, and their place was taken by tree shrews, mouse lemurs and owl monkeys (Martin 1976).
Habitus and habitat
Hystricomorphs are usually strict herbivores, although the type of diet varies (Ojeda et al. 2015). They tend to be gregarious animals, and some, such as the plains viscacha, form large colonies. Others, such as the paca, are solitary. There are both monogamous and polygamous species (Herrera 2015). There is a wide range of phenotypes as exemplified in Fig. 1.
Examples of hystricomorph rodents. A. Plains viscacha (Lagostomus maximus: Chinchillidae). Body length excluding tail (BL) 50–60 cm. B. Red-rumped agouti (Dasyprocta leporina: Dasyproctidae). BL 50–60 cm. C. Indian crested porcupine (Hystrix indica: Hystricidae). BL 70–90 cm. D. Talas tuco-tuco (Ctenomys talarum: Ctenomyidae). BL 21–25 cm. Courtesy of © Evangelina Indelicato. E. Brazilian guinea pig (Caviaaperea: Caviidae). BL 27–30 cm. F. Capybara (Hydrochoerushydrochaeris: Caviidae). BL 100–130 cm. Images A–C and E–F from Wikipedia CC BY-SA.
Citation: Reproduction 166, 1; 10.1530/REP-23-0028
Examples of hystricomorph rodents. A. Plains viscacha (Lagostomus maximus: Chinchillidae). Body length excluding tail (BL) 50–60 cm. B. Red-rumped agouti (Dasyprocta leporina: Dasyproctidae). BL 50–60 cm. C. Indian crested porcupine (Hystrix indica: Hystricidae). BL 70–90 cm. D. Talas tuco-tuco (Ctenomys talarum: Ctenomyidae). BL 21–25 cm. Courtesy of © Evangelina Indelicato. E. Brazilian guinea pig (Caviaaperea: Caviidae). BL 27–30 cm. F. Capybara (Hydrochoerushydrochaeris: Caviidae). BL 100–130 cm. Images A–C and E–F from Wikipedia CC BY-SA.
Citation: Reproduction 166, 1; 10.1530/REP-23-0028
Examples of hystricomorph rodents. A. Plains viscacha (Lagostomus maximus: Chinchillidae). Body length excluding tail (BL) 50–60 cm. B. Red-rumped agouti (Dasyprocta leporina: Dasyproctidae). BL 50–60 cm. C. Indian crested porcupine (Hystrix indica: Hystricidae). BL 70–90 cm. D. Talas tuco-tuco (Ctenomys talarum: Ctenomyidae). BL 21–25 cm. Courtesy of © Evangelina Indelicato. E. Brazilian guinea pig (Caviaaperea: Caviidae). BL 27–30 cm. F. Capybara (Hydrochoerushydrochaeris: Caviidae). BL 100–130 cm. Images A–C and E–F from Wikipedia CC BY-SA.
Citation: Reproduction 166, 1; 10.1530/REP-23-0028
Hystricomorphs play essential roles in the ecology of various biomes in South America, for example through seed dispersal (Forget 1990). Thus, reintroduction of the red-rumped agouti (Dasyprocta leporina) proved beneficial to dispersal of large seeds in a rewilding context (Mittelman et al. 2020). Small species like cavies and tuco-tucos are important items of diet for mammalian and avian predators (Weir & Rowlands 1973, Zapata & Procopio 2015). Some have been regarded as agricultural pests. The plains viscacha (Lagostomus maximus), for example, competes for forage with cattle, and some cavies feed on cultivated vegetables. Because of their digging behaviour, viscachas and tuco-tucos are said to cause environmental damage (Jackson 1988). On the other hand, the burrowing activity of tuco-tucos helps maintain the vegetation and soil of natural grasslands (Malizia et al. 2000). Some hystricomorph rodents are important as reservoirs for zoonotic diseases (Jones 2022). Finally, in both a traditional and a modern context, some are a source of food. In West Africa, the greater cane rat or grasscutter (Thryonomys swinderianus) is prized for its meat (Asibey 1974a , Jori et al. 1995, Yapi et al. 2021). The guinea pig is still considered a delicacy in Peru (Pritt 2012, Defrance 2021), and the meat of larger species such as capybara (Hydrochoerus hydrochaeris), viscacha, paca (Cuniculus paca) and agouti (Dasyprocta spp.) is consumed in some parts of South America. Capybara, paca and agouti are bred in captivity in some countries.
In recent years, these considerations have led to renewed study of the genomics, ecology and reproductive biology of hystricomorphs often led by South American scientists (Vassallo & Antenucci 2015, Gariboldi et al. 2019, Flamini et al. 2020, Barbeito et al. 2021).
Taxonomy
Hystricomorpha is a suborder of rodents comprising some 78 genera and 307 species (Burgin et al. 2018, American-Society-of-Mammalogists 2002). It was defined by morphological characters especially the very large intraorbital foramen that accommodates most of the medial masseter muscle (hystricomorphy) (Kelt & Patton 2020). Many taxonomic issues within the suborder were unresolved at the time of the 1973 symposium (see below), but greater clarity has emerged in the era of phylogenetics (Huchon & Douzery 2001, Opazo 2005, Rowe et al. 2010). Thus, we now have a much firmer picture of the relations between its clades (Fig. 2).
Phylogenetic tree for the rodent suborder Hystricomorpha based on a summary of current opinion by Kelt and Patton (Kelt & Patton 2020). Infraorder Ctenodactylomorphi (families in green) comprises Laotian rock rat and gundies. Infraorder Hystricognathi is traditionally divided into the monophyletic Caviomorpha (families in blue) from South America and the paraphyletic Phiomorpha (families in black) from Asia and Africa.
Citation: Reproduction 166, 1; 10.1530/REP-23-0028
Phylogenetic tree for the rodent suborder Hystricomorpha based on a summary of current opinion by Kelt and Patton (Kelt & Patton 2020). Infraorder Ctenodactylomorphi (families in green) comprises Laotian rock rat and gundies. Infraorder Hystricognathi is traditionally divided into the monophyletic Caviomorpha (families in blue) from South America and the paraphyletic Phiomorpha (families in black) from Asia and Africa.
Citation: Reproduction 166, 1; 10.1530/REP-23-0028
Phylogenetic tree for the rodent suborder Hystricomorpha based on a summary of current opinion by Kelt and Patton (Kelt & Patton 2020). Infraorder Ctenodactylomorphi (families in green) comprises Laotian rock rat and gundies. Infraorder Hystricognathi is traditionally divided into the monophyletic Caviomorpha (families in blue) from South America and the paraphyletic Phiomorpha (families in black) from Asia and Africa.
Citation: Reproduction 166, 1; 10.1530/REP-23-0028
The current consensus places gundis and the Laotian rock rat (Laonastes aenigmamus) in infraorder Ctenodactylomorphi and thus distinct from all other species, which are placed in infraorder Hystricognathi. Gundis are small desert rodents from northern Africa that live in colonies on rocky terrain (George 1974). The Laotian rock rat, from the karst formations of Central Laos, is a relict species first described in 2005 (Dawson et al. 2006).
Hystricognathi comprises five families from Africa and Asia (Phiomorpha) and ten from South America (Caviomorpha). Caviomorpha is monophyletic, and most authorities accept that a founding population reached South America in the Middle Eocene (Antoine et al. 2012) probably crossing the South Atlantic by rafting (Rowe et al. 2010). There followed a broad and successful radiation (Carter & Mess 2013). We here focus on current research on South American hystricomorph rodents, much of which has been done in their countries of origin.
Biographies
Barbara Jill Weir
Barbara Weir (Fig. 3) was born on 17 January 1942 at Upper Bentley, Worcestershire. She was educated at Loughton County High School for Girls and Girton College, Cambridge. She began her postgraduate work at the Marshall Laboratory in Cambridge and moved to the Wellcome Institute of Comparative Zoology with her supervisor I. W. Rowlands. Her dissertation, ‘Some aspects of reproduction in hystricomorph rodents’, was completed in 1968 after which she stayed at the Institute as a Ford Foundation Research Fellow. To start with, few specimens other than chinchilla (Chinchilla lanigera) were available for study. Therefore, together with Rowlands, she made two trips to South America to trap hystricomorphs, first in 1967 and then in 1970. The latter trip comprised of 6 weeks in Argentina and 2 each in Bolivia and Peru (Rowlands 1972). On her return, she went about establishing breeding colonies and husbandry practices as detailed below.
Barbara J Weir. Reproduced with permission from (Rowlands 1994) © Journals of Reproduction and Fertility Ltd.
Citation: Reproduction 166, 1; 10.1530/REP-23-0028
Barbara J Weir. Reproduced with permission from (Rowlands 1994) © Journals of Reproduction and Fertility Ltd.
Citation: Reproduction 166, 1; 10.1530/REP-23-0028
Barbara J Weir. Reproduced with permission from (Rowlands 1994) © Journals of Reproduction and Fertility Ltd.
Citation: Reproduction 166, 1; 10.1530/REP-23-0028
In 1973, Barbara Weir’s fellowship ended, and her career took a new direction. She was appointed assistant editor of Journal of Reproduction and Fertility (now Reproduction) and from 1976 executive editor, a post she held for some 20 years. She was a fair and firm editor, although it was noted that her meticulousness could bring her into conflict with authors (Rowlands 1994, Anonymous 1995).
Barbara Weir was a dedicated sportswoman. She earned Cambridge University Blues in cricket, hockey and swimming (Girton-College-Archive) and later was a much-respected hockey referee. When ill health forced her to abandon this strenuous pursuit, she took up golf and became proficient, landing three holes-in-one (Cambridge Evening News 1994). She was a keen gardener, and her home in Hauxton was described as a haven of rest and relaxation (Anonymous 1995). She died there on 22 December 1993, aged only 51, following a relapse of her chronic illness.
Idwal Wyn Rowlands
I W Rowlands was Barbara Weir’s supervisor for her Cambridge PhD as well as co-organizer of the Symposium. He was born 31 August 1908 at St Asaph, Denbighshire, Wales. He began his career at Bangor University under the tutelage of F. W. Rogers Brambell FRS (1901–1970). In 1933, he joined A. S. Parkes at the National Institute for Medical Research, Hampstead. During World War II, he was seconded to the Wellcome Veterinary Research Station at Frant, Sussex, as part of a team developing a vaccine against scrub typhus (Buckland & Dudgeon 1945). He retained a connection with Frant after moving to the ARC Institute of Animal Physiology at Babraham, Cambridge. In 1964, Parkes persuaded the Wellcome Trust to fund the Institute of Comparative Physiology at the ZSL, and he recommended the appointment of Rowlands, ‘his old friend and colleague’,, as its first director (Polge 2006). Rowlands remained in this position from 1964 until his retirement in 1974 (Martin 1976). He then returned to Cambridge where he remained active until well into his eighties.
Rowlands’ research interests were eclectic and by no means restricted to hystricomorph rodents. They encompassed the reproductive biology of a variety of laboratory, zoo and feral mammals. The last included the bank vole (Clethrionomys glareolus) (Brambell & Rowlands 1936) and several species of seal (Amoroso et al. 1951). He did early work on pregnant mare serum gonadotropin (Rimington & Rowlands 1943) and maintained a lifelong interest in equine reproduction: his last publication was as editor of a symposium in the field (Wade et al. 1991). Rowlands died at age 96 on 24 January 2005.
Evolution and taxonomy of hystricomorph rodents
Strikingly, at the 1973 symposium, two experts on taxonomy failed to agree on the relation between the African and South American species and both agreed to exclude the gundis (Lavocat 1974, Wood 1974). As noted above, molecular phylogenetics has since resolved those issues.
Barbara Weir’s interest in taxonomy was reflected in her studies of hystricomorph chromosomes and her attempts to determine the origin of the domestic guinea pig.
Hystricomorph chromosomes
Prior to the molecular era, karyotype patterns were analysed to elucidate phylogenetic relationships (George & Weir 1974). It was thought that chromosome rearrangements played a role in speciation, as evidenced by the pioneering studies of Osvaldo Reig (1929–1992) in tuco-tucos (Reig & Kiblisky 1969). A project undertaken by Weir and Wilma George (1918–1989) of Lady Margaret Hall, Oxford, was a study of hystricomorph chromosomes. Initial reports concerned the karyotype of cavies, the Talas tuco-tuco (Ctenomys talarum), the common degu (Octodon degus) and mountain degu (Octodonomys gliroides) (George et al. 1972, George & Weir 1972a ). In addition, a high chromosome number (2n = 88) was reported for the Jamaican hutia (Geocapromys brownii) (George & Weir 1972b ). The record was later broken when the red viscacha rat (Tympanoctomys barrerae) was shown to have a diploid number of 2n = 102 (Contreras et al. 1990), but this was not far from the ancestral chromosome number (2n = 98) arrived at by George and Weir (George & Weir 1974). Their analysis comprised their own and literature data from 41 hystricomorph rodents on diploid number, the fundamental number, proportion of metacentric chromosomes, satellite chromosomes and sex chromosomes. Among their conclusions were a close relationship (a) between Caviidae and Dasyproctidae and (b) between Octodontidae, Ctenomyidae, Echimyidae and Capromyidae (George & Weir 1974). These inferences are largely in agreement with recent molecular trees (Huchon & Douzery 2001, Rowe et al. 2010).
Origins of the guinea pig
Barbara Weir was interested in the origins of the domestic guinea pig as it does not occur in the wild. She studied some of its relatives both in the field and in a laboratory setting (Rood & Weir 1970, Weir 1974b ) but did not reach a definitive conclusion. Recent genomic analyses point to the montane guinea pig (Cavia tschudii) as the closest relative. Specimens from Ica, Peru (Cavia t. tschudii), and domestic animals (C. porcellus) form a sister clade to other C. tschudii subspecies (Spotorno et al. 2007, Dunnum & Salazar-Bravo 2010). An origin of domestic from montane guinea pigs receives further support from analysis of their chromosomes (Walker et al. 2014).
Hystricomorph rodents as laboratory animals
Weir established breeding colonies of mainly South American species and made recommendations on husbandry that were summarized in two excellent handbook chapters (Weir 1976a , 1976b ) (Table 1). Papers on husbandry include advice on chinchilla, red-rumped agouti, green acouchi (Myoproctor pratti) and African crested porcupine (Hystrix cristata) (Weir 1967); on cavies, common degu and plains viscacha (Weir 1970) and on casiragua (Proechimys guairae) (Weir 1973a ). Other species kept at the laboratory were mountain degu (Octodontomys gliroides) and Jamaican hutia (Geocapromys brownii) (Rowlands 1972). The group is exemplified here with the chinchillids and the Talas tuco-tuco (Ctenomys talarum), the latter as an example of the limitations to captive breeding. The domestic guinea pig is well established as a laboratory animal, and advice on its husbandry should be sought in current handbooks (Suckow et al. 2012, Clemons et al. 2011).
Hystricomorph rodents maintained in the laboratory at the Wellcome Institute of Comparative Physiology with original source and references for husbandry.
| Common name(s) | Latin name | Family | Original source and notes | Husbandry |
|---|---|---|---|---|
| Crested porcupine | Hystrix cristata | Hystricidae | Nairobi (not bred in the laboratory) | Weir (1967) |
| Long-tailed or Chilean chinchilla | Chinchilla lanigera | Chinchillidae | Commercial fur breeders | Weir (1967, 1976a) |
| Plains viscacha | Lagostomus maximus | Chinchillidae | Pedro Luro, Argentina | Weir (1970, 1976b) |
| Brazilian guinea pig | Cavia aperea | Caviidae | Magdalena, Argentina | Weir (1970, 1976b) |
| Highland yellow-toothed cavy or Cuis | Galea musteloides | Caviidae | Cardenal Cagliero, Argentina | Weir (1970, 1976b) |
| Green acouchi | Myoproctor pratti | Dasyproctidae | Source not given, possibly London Zoo | Weir (1967, 1976b) |
| Red-rumped agouti | Dasyprocta leporina | Dasyproctidae | Dealer; mating not readily achieved | Weir (1967, 1976b) |
| Talas tuco-tuco | Ctenomys talarum | Ctenomyidae | Magdalena, Argentina; did not breed well in captivity | Weir (1974a , 1976b) |
| Common degu | Octodon degus | Octodontidae | Humahuaca, Argentina | Weir (1970, 1976b) |
| Mountain degu or Chozchori | Octodontomys gliroides | Octodontidae | Humahuaca, Argentina | Rowlands (1972) |
| Coypu | Myocastor coypus | Echimyidae | Ministry of Agriculture, Norwich | Weir (1976b) |
| Guaira spiny-rat or Casiragua | Proechimys guairae | Echimyidae | Dr O A Reig, Venezuela | Weir (1973a), Lusty & Seaton 1978 |
| Jamaican hutia | Geocapromys brownii | Echimyidae (Capromyinae) | Kingston, Jamaica | Rowlands (1972) |
Chinchilla and viscachas
The long-tailed chinchilla (Chinchilla lanigera) is a medium-sized rabbit-like rodent that lives in rocky outcrops in the Andes. The chinchilla is bred for its fur, and commercial breeders were the source for the colonies at Cambridge and London (Weir 1967). It was noted that the wild population is small, and indeed the chinchilla is currently listed as an endangered species (Roach & Kennerley 2016). In addition to describing an appropriate caging system (Weir 1967), Barbara Weir developed techniques to improve breeding of chinchillas, including semen collection (Healey & Weir 1967) and induction of ovulation (Weir 1973b). The plains viscacha (Fig. 1A) and mountain viscacha (Lagidium viscacia) are close relatives of the chinchilla. Weir trapped 40 plains viscacha in Argentina and established a breeding colony where most animals were housed in pens and fed rat pellets and fresh vegetables (Weir 1970). She made observations on a pair of mountain viscacha caught in Argentina (Weir 1971) but did not establish a breeding colony.
Talas tuco-tuco
Tuco-tucos are small- to medium-sized rodents adapted for a subterranean lifestyle, although they leave their burrows to forage for roots and grasses. The Talas tuco-tuco (Fig. 1D) is found in eastern Argentina. Barbara Weir was anxious to establish a breeding colony of tuco-tucos and trapped numbers of them during both her trips to Argentina. Initially, they were housed in groups of three or four in plastic rat cages. Although pregnant animals gave birth in the laboratory, subsequent breeding success was very low. A slightly better result was achieved when two males and three females were housed in an earth tank, but these animals bore the scars of fighting, suggesting that 1.1 m2 was insufficient for even a small number of tuco-tucos. The conclusion was that tuco-tucos could not be bred as a useful animal model (Weir 1974a).
Reproductive biology and endocrinology of hystricomorph rodents
An important part of the symposium was devoted to reproduction. This is unsurprising in the light of Barbara Weir’s contributions: she described reproduction in several species, some for the first time. The colony at the ZSL also provided embryos for postgraduate work by Christine Roberts (Roberts & Perry 1974). Research at Babraham and elsewhere focussed on the guinea pig. In addition, a paper was presented on reproduction in the greater cane rat (Asibey 1974b).
General aspects
Reproduction in hystricomorph rodents is characterized by a long gestation, a long oestrous cycle, a tendency to form accessory corpora lutea and a vaginal closure membrane that is present until oestrus (Weir & Rowlands 1973, 1974, Weir 1974c). The length of gestation is unusual for mammals of relatively small body size and in several cases even longer than in the guinea pig (68 days). An example is the plains viscacha (154 days). Often, the young are precocial at birth with open eyes and a full coat of hair, but the young of some species, such as tuco-tucos and the common degu, are less advanced and born with their eyes closed. Litter size varies, but several species can deliver up to six young. This contrasts with ungulates and primates, which also have long gestations but usually singleton or twin pregnancies.
There are distinctive features of implantation and placentation, as discussed at the 1973 symposium (Roberts & Perry 1974). The blastocyst becomes embedded deep in the decidual mucosa (interstitial implantation), and there is complete inversion of the germ layers (Kaufmann & Davidoff 1977). The parietal yolk sac comes to clothe part of the placental disk, and the visceral yolk sac forms a choriovitelline placenta that persists through term (Fig. 4A, B and C). The chorioallantoic placenta is discoid and labyrinthine with a single layer of syncytiotrophoblast in the interhaemal barrier (haemomonchorial). There is a characteristic lobular arrangement of the placenta that is apparent in cross-section (Fig. 4C) and is due to investment of lobules of labyrinth (the exchange areas) by interlobular trophoblast. A unique feature is the subplacenta (Fig. 4D), a specialized zone between the placental disc and basal decidua that is the source of invasive trophoblast (Davies et al. 1961, Mess et al. 2007). A subplacenta is not found in gundis (Mess 2003) or the Laotian rock rat (Carter et al. 2013), and so strictly speaking it is a feature of Hystricognathi, but it is present in African as well as South American species (Luckett & Mossman 1981).
Placentation in the capybara (Hydrochoerus hydrochaeris: Caviidae) at around 70 days gestation. A. Schematic drawing showing the thin capsular decidua (cd), visceral yolk sac (vys), amnion (am), main placenta (mp), subplacenta (sub), basal decidua (bd) and uterine cavity (uc). B. Gross morphology: the capsular decidua has been opened and reflected to expose the fetal membranes. The amnion has also been cut open but retains its attachment to the surface of the placental disc (arrowhead). The visceral yolk sac inserts more peripherally (arrow). The yolk sac vessels terminate in the sinus terminalis (asterisk). C. Section through placental disk (haemotoxylin and eosin). The lobules of the labyrinth (lab) are separated by interlobular areas of trophoblast supplied only by maternal vessels (int). This view also shows the relations between parietal yolk sac, visceral yolk sac and fibrovascular ring (fvr). D. Section through the subplacenta (haemotoxylin and eosin). It is situated beneath the main placenta and within the basal decidua. Scale bars = 1 cm (A), 1.5 mm (C and D). Reproduced from Kanashiro et al. (Kanashiro et al. 2009) © the authors CC BY 2.0.
Citation: Reproduction 166, 1; 10.1530/REP-23-0028
Placentation in the capybara (Hydrochoerus hydrochaeris: Caviidae) at around 70 days gestation. A. Schematic drawing showing the thin capsular decidua (cd), visceral yolk sac (vys), amnion (am), main placenta (mp), subplacenta (sub), basal decidua (bd) and uterine cavity (uc). B. Gross morphology: the capsular decidua has been opened and reflected to expose the fetal membranes. The amnion has also been cut open but retains its attachment to the surface of the placental disc (arrowhead). The visceral yolk sac inserts more peripherally (arrow). The yolk sac vessels terminate in the sinus terminalis (asterisk). C. Section through placental disk (haemotoxylin and eosin). The lobules of the labyrinth (lab) are separated by interlobular areas of trophoblast supplied only by maternal vessels (int). This view also shows the relations between parietal yolk sac, visceral yolk sac and fibrovascular ring (fvr). D. Section through the subplacenta (haemotoxylin and eosin). It is situated beneath the main placenta and within the basal decidua. Scale bars = 1 cm (A), 1.5 mm (C and D). Reproduced from Kanashiro et al. (Kanashiro et al. 2009) © the authors CC BY 2.0.
Citation: Reproduction 166, 1; 10.1530/REP-23-0028
Placentation in the capybara (Hydrochoerus hydrochaeris: Caviidae) at around 70 days gestation. A. Schematic drawing showing the thin capsular decidua (cd), visceral yolk sac (vys), amnion (am), main placenta (mp), subplacenta (sub), basal decidua (bd) and uterine cavity (uc). B. Gross morphology: the capsular decidua has been opened and reflected to expose the fetal membranes. The amnion has also been cut open but retains its attachment to the surface of the placental disc (arrowhead). The visceral yolk sac inserts more peripherally (arrow). The yolk sac vessels terminate in the sinus terminalis (asterisk). C. Section through placental disk (haemotoxylin and eosin). The lobules of the labyrinth (lab) are separated by interlobular areas of trophoblast supplied only by maternal vessels (int). This view also shows the relations between parietal yolk sac, visceral yolk sac and fibrovascular ring (fvr). D. Section through the subplacenta (haemotoxylin and eosin). It is situated beneath the main placenta and within the basal decidua. Scale bars = 1 cm (A), 1.5 mm (C and D). Reproduced from Kanashiro et al. (Kanashiro et al. 2009) © the authors CC BY 2.0.
Citation: Reproduction 166, 1; 10.1530/REP-23-0028
Some unique features of placentation discussed at the symposium have been described for further species. These include African hystricognaths such as the Namaqua dune mole rat (Bathyergus janetta), the Cape porcupine (Hystrix africaeaustralis) and the greater cane rat (Luckett & Mossman 1981, Oduor-Okelo & Gombe 1982, Oduor-Okelo 1984). More recently, a programme was initiated to study placentation in South American species (Miglino et al. 2004, Kanashiro et al. 2009), which led to an analysis of placental evolution in the hystricomorph clade (Franco de Oliveira et al. 2012).
Progesterone and progesterone-binding globulin
A long oestrous cycle is typical for caviomorphs but has also been shown for the African crested porcupine (Weir 1967, Weir & Rowlands 1973). The long life of the corpus luteum in the oestrous cycle has been linked to its role in the first weeks of pregnancy (Weir & Rowlands 1973). Eventually, it is replaced as a source of progesterone, either by accessory corpora lutea as in the acouchi (Rowlands et al. 1970), chinchilla (Tam 1971, 1972) and the North American porcupine (Erethizon dorsatum) (Mossman & Judas 1949) or by the placenta as in the guinea pig and cuis (Cavia aperea) (Heap & Deanesly 1966, Tam 1973). The functional anatomy of the ovary was reviewed at the symposium (Weir & Rowlands 1974), and progesterone synthesis was also discussed (Tam 1974). It was later shown in the guinea pig that placental progesterone synthesis occurs in the interlobular trophoblast (Tam 1977). The guinea pig resembles the human in that the placenta is a major source of progesterone with no change in plasma progesterone observed prior to parturition (Thorburn et al. 1977). Therefore, it is considered an appropriate model for research on pregnancy maintenance and parturition (Mitchell & Taggart 2009).
Progesterone levels are high during gestation due in part to increased secretion from ovarian and non-ovarian sources and in part to a low metabolic clearance rate. Clearance is low because most circulating progesterone is bound to a progesterone-binding globulin (PBG), as shown first for the guinea pig and degu (Heap & Illingworth 1974). PBG is unique to hystricomorph rodents; it is absent in murids, ferret, pig, sheep and human. PBG is secreted from the interlobular trophoblast of the placenta (Metz et al. 1977) and may have evolved to support the long gestation that characterizes hystricomorphs (Heap et al. 1981). However, the time course of plasma PBG concentration varies between species. There are two peaks in guinea pigs at 20–25 days and from 50 days to term (about 68 days); PBG peaks just before parturition in casiragua; and there is a mid-gestation peak in cuis, degu and plains viscacha (Heap et al. 1981). Subsequent work on the Cape porcupine showed an increase in PBG from 35 to 68 days, yet it was undetectable at 87 days (near term) (Louw et al. 1992).
Superovulation and fetal reabsorption
Some remarkable features of reproduction are known only for the plains viscacha. First, 200–800 eggs are ovulated at oestrus although most are not fertilized (Roberts & Weir 1973). Superovulation is not uncommon in marsupials (Harder et al. 1993), but among eutherians it is known only from the plains viscacha and some species of elephant shrew (Tripp 1971). As discussed in a later section, recent studies on ovaries of viscachas from different ontogenetic and reproductive stages have elucidated the mechanisms behind these unusual reproductive events.
Superovulation does not occur in chinchilla or mountain viscacha. In the latter species, however, ovulation nearly always occurs from the right ovary and a single fetus is carried in the right horn (Pearson 1949, Weir 1971). This pattern is known from several mammals including whales (Ohsumi 1964), bats (Rasweiler & Badwaik 2000) and deer (Child & Mossman 1965).
In the plains viscacha, up to five embryos may implant in each horn, but only those nearest the cervix survive whilst the remaining ones are resorbed (Roberts & Weir 1973). Although embryonic resorption is observed in other species such as chinchilla (Weir 1967) and coypu (Newson 1966), it is not as systematic as in the plains viscacha.
Trophoblast deportation
Trophoblastic deportation is the migration of the trophoblasts from the placenta to the maternal blood vessels and its spread to other organs, including the lungs (Pantham et al. 2011). It occurs in human pregnancy and in other mammals with haemochorial placentation. This was shown for chinchilla by Billington and Weir, who found groups of one to six trophoblastic cells irregularly distributed throughout the lungs (Billington & Weir 1967). Recently, we found large, irregular cells, positive for pancytokeratin and progesterone receptor antibodies, in the lungs of plains viscacha examined at 45 days of pregnancy. These were interpreted as evidence of trophoblastic deportation (Acuña et al. 2022b). Trophoblast deportation has also been described in a cricetid rodent, the hispid cotton rat (Sigmodon hispidus). There, trophoblast cells in the lung of pregnant females were associated with haemorrhage and pulmonary oedema, fibrinoid vascular necrosis, endothelial hypertrophy and abundant alveolar macrophages (La Perle et al. 2014).
Insulin and diabetes
Apart from reproduction, the endocrinology of hystricomorph rodents is characterized by several distinctive features of both the pituitary–adrenal axis and the gastro–entero–pancreatic axis (Keightley & Fuller 1996). These include an unusually large number of substitutions in the amino acid sequences of insulin (Smith 1966, Horuk et al. 1979, Chan et al. 1984, Bajaj et al. 1986).
Barbara Weir was keen to develop a model for diabetes in the Talas tuco-tuco, as apparent from press reports of her second expedition to South America (The Birmingham Post 1970). Initial findings were hyperglycaemia associated with the development of cataracts (Wise et al. 1968). This was shown to be diet dependent, suggesting tuco-tucos as a model for type II diabetes (Wise et al. 1972). As described above, this project failed because of difficulties encountered in breeding tuco-tucos in captivity.
Weir was also interested in hystricomorph insulins. It was known at the time that they differed from those of most other mammals (Smith 1966). To look further into this, Weir and colleagues examined the effect on blood glucose levels of neutralizing antibodies to beef/pork insulin (Neville et al. 1973, 1974). Whilst the yellow-toothed cavy and chinchilla became hyperglycaemic, no response was found in guinea pig, tuco-tuco, degu or casiragua. The response of the chinchilla correlated with fewer amino acid substitutions and greater biological potency (Horuk et al. 1979), but the difference in response of the two caviids was less easy to explain.
Legacy
Barbara Weir was the first to investigate the reproductive physiology of many species of hystricomorph rodent. The programme was discontinued when she became a full-time editor and Rowlands retired (Martin 1976). Work did continue for a while on the casiragua at the ZSL (Lusty & Seaton 1978) and on the cuis after transfer to Babraham (Norris & Adams 1979). The guinea pig continues to be important for research in reproduction; its present status as a model is reviewed elsewhere (Mitchell & Taggart 2009, Carter 2020, Candia et al. 2023). We here focus on current research on South American hystricomorph rodents, much of which has been done in their countries of origin.
Chinchilla
Commercial breeding of chinchilla for its pelt is still widespread, yet publications on its reproductive physiology have been sporadic. An example is a recent description of the uterine vasculature (Cevik-Demirkan et al. 2010), An interesting development has been non-invasive monitoring of ovarian and adrenal hormones by measuring their urinary metabolites. Applied to pregnancy, parturition and the postpartum period, such studies confirm a decline in progesterone secretion towards term and a surge in luteinizing hormone after parturition in keeping with postpartum oestrus (Mastromonaco et al. 2015). Recently, chinchilla was proposed as a model for pregnancy research, and the fetus and placenta were studied by advanced imaging techniques (Mikkelsen et al. 2017, Greco et al. 2019, Overgaard et al. 2019). These allowed placental pyruvate metabolism to be followed in real time (Mikkelsen et al. 2017) and also established that the antidiabetic drug metformin does not cross the chinchilla placenta to the fetus (Overgaard et al. 2019).
Plains viscacha
In recent decades, various research groups in Argentina have studied the morphological, functional and molecular aspects of reproduction in plains viscacha using animals trapped in the wild rather than raised in breeding colonies. Thus, research has been done on the pineal gland and the photoperiod as well as on seasonal variations in male reproduction and the characteristics of the endocrine glands (Filippa et al. 2015, Busolini et al. 2017). Several groups have addressed polyovulation, pregnancy maintenance and fetal loss in the plains viscacha. Maintenance of a large pool of primary oocytes and of large numbers of corpora lutea can be ascribed in part to upregulation of the apoptosis-inhibiting Bcl2 gene and downregulation of the apoptosis-promoting Bax gene (Jensen et al. 2008, Leopardo et al. 2011). The role of the hypothalamic–pituitary–ovarian axis has been documented in some detail both for the initial ovulation and the mid-gestation appearance of secondary corpora lutea. The secondary corpora lutea are derived by luteinization of non-ovulatory follicles, but there is also evidence of new primary corpora lutea arising through ovulation at mid-gestation (Jensen et al. 2008, Dorfman et al. 2013). A decrease in circulating progesterone at mid-gestation reactivates the hypothalamic–pituitary–ovarian axis and additionally boosts progesterone secretion from the existing primary corpora lutea to restore progesterone levels (Cortasa et al. 2022). Others have focussed on the reproductive organs of the female, highlighting the changes that occur at different reproductive stages (Flamini et al. 2009, 2012, 2014, 2019, 2020). The finding of an active female prostate in plains viscacha stands out (Flamini et al. 2002, 2021). This gland has not been described in any other rodent of the group, although it is known from non-hystricomorph rodents such as the brown rat (Rattus norvegicus) and Mongolian gerbil (Meriones unguiculatus).
Different studies have recently been carried out to explore some aspects of polyimplantation and embryonic death in the plains viscacha. Weir concluded that early embryonic death in the plains viscacha could not be explained by morphological variations in the uterine horns or by aetiological agents (Roberts & Weir 1973). Recent studies, in non-pregnant females, showed that the uterine segments corresponding to those where resorption occurs have significantly smaller glandular and vascular areas compared to the caudal segments where viable implantations site are found (Acuña et al. 2020). In females with early and intermediate gestations, a relationship was established between these morphological variations in the uterine horns and embryonic death (Acuña et al. 2021, 2022a).
Talas tuco-tuco
Another South American species that interested Weir was the Talas tuco-tuco. Currently, several research groups from Argentina study these subterranean caviomorphs. Their physiology and behaviour have been explored by transferring live-trapped individuals to artificial burrows. This has enabled the study of the energetics of pregnancy and lactation, which is of interest since tuco-tucos are altricial at birth (Zenuto et al. 2002). An attempt was made to breed tuco-tucos in captivity, although with little more success than achieved by Weir (Weir 1974a). An enclosure was designed where two males and three females each had an artificial burrow 3.5 m long. Individual territories were established but not without conflict between males that led to physical injury. The dominant male mated with all three females, but this resulted in only one successful pregnancy (Zenuto et al. 2001). In later work, mating behaviour between a single male and female was observed in a test chamber, but in experiments of relatively short duration (Fanjul & Zenuto 2008). To study male dominance, interactions between males were limited to 20 min (Fanjul & Zenuto 2017) and to determine how dominance affected a female’s choice, she was exposed to tethered males or their odours (Fanjul & Zenuto 2017). Weir reported the occurrence of hyperglycaemia in this species (Weir 1974a). Therefore, it is pertinent to note that blood glucose levels in the field were within the normal range for mammals. although, based on glucose tolerance tests, it was found that tuco-tucos had a diminished capacity to regulate blood glucose (Vera et al. 2008).
Capybara and lowland paca
Some hystricomorph rodents are too large to be kept in the laboratory though they can be housed in pens. The capybara (Fig. 1F) is by far the biggest with an adult weight of up to 55 kg but nevertheless has been used in studies of reproduction and placentation (Kanashiro et al. 2009, Miglino et al. 2013). The second largest species, the lowland paca, is also studied (Bonatelli et al. 2005, Greco et al. 2019, Uscategui et al. 2021).
Conclusions
There has been a resurgence of interest in the biology of hystricomorph rodents, especially in South America, where they are a conspicuous part of the fauna in diverse biomes (Vassallo & Antenucci 2015). Part of this research focuses on their reproduction, which is unique among rodents in several respects (Miglino et al. 2013, Acuña et al. 2022a). Although the domestic guinea pig was an established laboratory animal, little was known about reproduction in other hystricomorphs until the seminal studies by Barbara Weir. Her research programme culminated 50 years ago with a symposium at the ZSL and the resultant publication of its proceedings (Rowlands & Weir 1974). Weir’s work and that of her mentor I. W. Rowlands remains the starting point and benchmark for all current research on the reproductive biology of this interesting suborder of rodents.
Declaration of interest
The authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of this review.
Funding
F A and C B are grateful to CONICET and UNLP for grants to support several studies in the plains viscacha (Lagostomus maximus).
Author contribution statement
A C conceived the topic. A C, F A and C B contributed equally to reviewing the literature and to writing and revising the manuscript.
Acknowledgements
The authors are grateful to Ms Hannah Westall, Archivist and Curator, Girton College, Cambridge, for access to the personal papers of Barbara Weir. F A and C B are grateful to Dra. Mirta A. Flamini (FCV-UNLP) for introducing them to the study of hystricomorph rodents. Evangelina Indelicato kindly provided a photo of the Talas tuco-tuco. The authors thank Professor Aldo I. Vassallo and two anonymous reviewers for incisive comments on a previous version of the manuscript.
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