The reproductive rates of Australian rodents

Summary The reproductive rates of about 50 species of Australian rodents were studied by calculating allometric equations for the relationships between female body weight, litter size, length of gestation and weaning periods as well as age of sexual maturity.Members of the subfamily Hydromyinae, which invaded Australia 5–10 million years ago, are characterised by small litters, long gestation and weaning periods and late maturity. The opposite is true for the Murinae (Rattus and Mus) which invaded Australia during the Pleistocene. Among the species of this latter group, those which invaded earlier have reproductive rates closer to the old invaders, while those which arrived with the Europeans during the last 200 years have the highest reproductive rates.Possible reasons for the low reproductive rates of Australian rodents are discussed. It is concluded that the rain forest origin of the hydromyinids is one of the factors responsible for their low reproductive rate. They maintained this rate to the present time because of the unpredictability of the climate and the low productivity of many Australian habitats.     

The development of small primate models for aging research

Nonhuman primate (NHP) aging research has traditionally relied mainly on the rhesus macaque. But the long lifespan, low reproductive rate, and relatively large body size of macaques and related Old World monkeys make them less than ideal models for aging research. Manifold advantages would attend the use of smaller, more rapidly developing, shorter-lived NHP species in aging studies, not the least of which are lower cost and the ability to do shorter research projects. Arbitrarily defining "small" primates as those weighing less than 500 g, we assess small, relatively short-lived species among the prosimians and callitrichids for suitability as models for human aging research. Using the criteria of availability, knowledge about (and ease of) maintenance, the possibility of genetic manipulation (a hallmark of 21st century biology), and similarities to humans in the physiology of age-related changes, we suggest three species--two prosimians (Microcebus murinus and Galago senegalensis) and one New World monkey (Callithrix jacchus)--that deserve scrutiny for development as major NHP models for aging studies. We discuss one other New World monkey group, Cebus spp., that might also be an effective NHP model of aging as these species are longer-lived for their body size than any primate except humans.     

Primate spermatogenesis: new insights into comparative testicular organisation, spermatogenic efficiency and endocrine control

Owing to the close phylogenetic relationship of Platyrrhini (New World monkeys) and Catarrhini (Old World monkeys) to man, nonhuman primates are often used as models for the study of male reproductive physiology and endocrinology. This review aims at providing new data and insights into comparative primate spermatogenesis, dealing specifically with quantitative aspects of germinal epithelial organisation and germ cell production, and with the roles of gonadotrophic hormones in this process. Typically, the seminiferous epithelium is composed of specific germ cell associations (spermatogenic stages). In rodents, prosimians and most Catarrhini, tubular cross sections contain a single spermatogenic stage whereas in Platyrrhini, great apes and man multi-stage tubules are present. Since Platyrrhini represent a more basal type of primate, this spermatogenic feature must have developed convergently. The primate multi-stage tubular arrangement was previously believed to be associated with low spermatogenic efficiency. However, recent studies using new methodological approaches and comparing primate species from all taxa have revealed that multistage organisation is compatible with highly efficient spermatogenesis. In fact, meta-analysis demonstrated that the efficiency of spermatogenesis in several nonhuman primate species is comparable to that of rodents which are considered as species with highly efficient germ cell production. The duration of the spermatogenic process was not related to organisation or efficiency of spermatogenesis. Sertoli cell work load was species-specific but had no impact on germ cell numbers and on the efficiency of spermatogenesis. The gonadotrophic hormones, luteinizing hormone (LH) and follicle stimulating hormone (FSH) are the primary regulators of primate testicular function. Recent studies revealed that in New World monkeys chorionic gonadotrophin (CG)--the primate pregnancy hormone--regulates testosterone production instead of LH. Receptor studies demonstrated a dual action of the closely related hormones LH and CG in primates. It is hypothesised that following the divergence of the Platyrrhini lineage from Catarrhini, the LH/CG system evolved independently with ancestral functions of the LH/CG system retained in the neotropical taxa. In summary, key spermatogenic features are preserved across all primate taxa whereas male reproductive endocrinology features appear substantially different in the neotropical primates compared to other primate lineages.     

Seasonal Regulation of Reproduction in Muroid Rodents

This paper offers a conceptual scheme dealing with the way environmentalfactors influence reproduction in muroid rodents. The combinationof small size, short life span, and the fact that most environmentsare relatively unpredictable for short-lived animals, suggeststhat opportunism must be a key element in the reproductive strategiesof most of these animals. Flexibility is assured by the useof dynamically changing multiple reproductive strategies withinpopulations, simultaneous multiple cueing in individuals, modificationof an individual's responses to these cues by earlier experiences,and the use or lack of use of predictors of different kinds.     

The nut-crackers – a new theory of the adaptations of the Ramapithecinae

Molar enamel is thicker among frugivorous extant Old World monkeys and apes than among their folivorous close relatives. Furthermore, species that have the thickest molar enamel reportedly eat fruits, seeds, and nuts that are so hard that they cannot be broken by their sympatric thinner-enameled relatives. Species with relatively thick enamel show no tendency toward a terrestrial feeding pattern. Members of the Ramapithecinae, the stock which probably gave rise to Pliocene-Recent hominids, had very thick molar enamel. This suggests that they ate hard seeds, nuts, and fruits previously available only to arboreal rodents and forest-floor pigs. There is no reason to believe that these anatomical features had to evolve in non-rain-forest environments, as others have argued.     

Structure of the reproductive system of the squid Thysanoteuthis rhombus (Cephalopoda: Oegopsida)

The structure of the reproductive systems of mature males and females of the nektonic, oceanic squid Thysanoteuthis rhombus are described. The main peculiarities of the female system are relatively low capacity oviducts, set in a tight spiral, and hypertrophically developed oviducal glands with a very large second section. The male reproductive system is characterized by a long, narrow Needham's sac containing 10–15 large spermatophores 80–100 mm in length. The mesentery supporting the gonad, and protruding into it dorsally, is a characteristic feature in both sexes. The hectocotylus structure differs markedly from that in other squids and resembles that of sepiids. The reproductive system of T. rhombus possesses primitive features (pattern of gonad attachment and hectocotylus) but mostly secondary characters (small oviducts, very large oviducal glands and ovary). The complex morpho-ecological adaptations of T. rhombus are reflected in the distinctive features of the reproductive system.     

Pre- and postnatal growth of the Cape porcupine Hystrix africaeaustratis

Pre- and postnatal growth of the Cape porcupine Hystrix africaeaustralis is evaluated by means of the Huggett & Widdas equation, a modification thereof, and the von Bertalanffy equation. Specific foetal growth velocity for the Cape porcupine is higher than that recorded for most other hystricomorph rodents, but similar to that recorded for large-bodied rodents of the same group. Relatively high foetal growth velocity in porcupines is ascribed to their relatively short gestation period, the latter being longer than expected for mammals of equal size, but shorter than expected for a hystricomorph rodent.
Postnatal growth is nearly linear up to the age of 20 weeks and asymptotic body weight is attained at an age of 52 weeks, this coinciding with the observed age at sexual maturity. Growth rates of males and females are similar. Their high rate of postnatal growth and development results in an extended reproductive period, thereby enhancing individual reproductive values by counteracting the effects of seasonal breeding and small litter size.     

Geometry and evolutionary parallelism in the long bones of cavioid rodents and small artiodactyls

Morphological parallelism between South American cavioid rodents and small artiodactyls from the Old World has been postulated for a long time. Our study deals with this question from the point of view of biomechanical characteristics of the long bones. For this, cross-sectional area, second moment of the area, polar moment, athletic ability indicators and strength were calculated for the long bones (i.e. humerus, radius, femur and tibia) of five species of cavioids and two species of artiodactyls. Regressions of all these variables to body mass were established. Regarding the cross-sectional area, the confidence intervals show that the exponents calculated are not significantly different from the geometrical predicted value. The exponents obtained for the second moment of area and the polar moment are not significantly different from the geometrical prediction, except for the humerus. The two indicators of athletic ability scaled as expected, but the bending indicator of athletic ability of the femur was not correlated to body mass. The exponent calculated for femur strength is not different from zero, while the strength of the humerus decreases slightly with the body mass. Additional statistical tests (ANCOVAs) showed no difference between the values of these variables calculated for the samples studied of artiodactyls and rodents. The present results are consistent with the hypothesis that there is significant evolutionary parallelism between cavioid rodents and small artiodactyls.     

Why do populations of small rodents cycle? A new hypothesis with numerical model

Summary A hypothesis for explaining the mechanism population of cycles in small rodents and the phenomena associated with these cycles is presented and supported by a numerical model. In strongly seasonal environments, with high reproductive ability and low mortality of rodents, the population size increases to a point at which either females refrain from breeding for the entire season or progeny of these females do not survive to produce their own progeny and a large proportion of animals die of old age. This brings about a population crash. The amplitudes of the cycles are high due to dispersal of animals without home ranges to the habitat which is only seasonably available and back to permanently available habitat. Without high reproductive abilities of animals and their good survival, only annual fluctuations are possible. Seven wellknown features of the cyclic populations are explained by the model and eight new predictions concerning these populations are given. The relations to other hypotheses are discussed briefly.     

The Gerbil Spermatozoon – interspecific variation in morphology does not invariably follow murine rodent evolutionary trends in response to predicted intermale sperm competition

In various groups of mammals, the intensity of intermale sperm competition relates to relative testes mass (RTM) with some evidence suggesting that this may also be the case for some aspects of sperm form. In murid rodents, a large RTM generally correlates with a streamlined sperm head, long apical hook and long tail with most data coming from species in the subfamily Murinae. In this study, RTM and sperm form are compared across 15 species of gerbils, seven from the Tribe Taterillini and eight from the Tribe Gerbillini. Marked interspecific differences in RTM and sperm morphology were observed. However, the Gerbilliscus species with the largest RTM do not have a sperm head with an apical hook nor a longer sperm tail than other species with smaller RTM whereas, by contrast, in the Tribe Gerbillini, species where the sperm head lacks a hook have a relatively small testes mass. We thus suggest that in gerbils, unlike in murine rodents, high levels of postcopulatory sexual selection have not invariably resulted in the evolution of a spermatozoon with a long apical hook and long sperm tail. The possible reasons for this are briefly discussed.     

A personal computer system for observation and analysis of copulatory behavior in small rodents

A personal computer system was developed for measuring values of copulatory behavior of small laboratory rodents. This system enabled us to get the analysis data of copulatory behavior of male rats as soon as possible after observation. This present system could be useful to measure other reproductive behavior of small rodents.     

Not putting all their eggs in one basket: bet‐hedging despite extraordinary annual reproductive output of desert tortoises

Bet‐hedging theory makes the counter‐intuitive prediction that, if juvenile survival is low and unpredictable, organisms should consistently reduce short‐term reproductive output to minimize the risk of reproductive failure in the long‐term. We investigated the long‐term reproductive output of an Agassiz's desert tortoise (Gopherus agassizii) population and conformance to a bet‐hedging strategy of reproduction in an unpredictable but comparatively productive environment. Most females reproduced every year, even during periods of low precipitation and poor germination of food plants, and the mean percentage of reproducing females did not differ significantly on an annual basis. Although mean annual egg production (clutch size × clutch frequency) differed significantly among years, mean clutch size and mean clutch frequency remained relatively constant. During an El Niño year, mean annual egg production and mean annual clutch frequency were the highest ever reported for this species. Annual egg production was positively influenced by maternal body size but clutch size and clutch frequency were not. Our long‐term results confirm earlier conclusions based on short‐term research that desert tortoises have a bet‐hedging strategy of producing small clutches almost every year. The risk of long‐term reproductive failure is minimized in unpredictable environments, both through time by annually producing multiple small clutches over a long reproductive lifespan, even in years of low resource availability, and through space by depositing multiple annual clutches in different locations. The extraordinary annual reproductive output of this population appears to be the result of a typically high but unpredictable biomass of annual food plants at the site relative to tortoise habitat in dryer regions. Under the comparatively productive but unpredictable conditions, tortoises conform to predictions of a bet‐hedging strategy of reproduction with relatively small but consistent clutch sizes. Published 2015. This article is a U.S. Government work and is in the public domain in the USA, Biological Journal of the Linnean Society, 2015, 115 , 399–410.     

Reproductive responses of temperate and boreal Tengmalm's Owl Aegolius funereus populations to spatial and temporal variation in prey availability

Environmental variation across space and time can strongly influence life‐history strategies in vertebrates. It has been shown that the reproductive success of birds of prey is closely related to food availability. However, relatively little is known about intraspecific differences in reproductive success of birds in relation to varying ecological conditions across environmental gradients. We investigated the reproductive performance of Tengmalm's Owls Aegolius funereus in a temperate (Czech Republic, 50°N) and a boreal (Finland, 63°N) population in relation to long‐term variations in the abundance of their main prey (small rodents). Prey densities at the northern site were much higher, but there were also large inter‐annual fluctuations and years with steep summer declines of vole densities. Northern owls laid larger clutches but offspring production per nest was similar at both study sites. This resulted from higher nestling mortality in the northern population, especially in nests established later in the season. Despite much greater nesting losses due to predation by Pine Martens Martes martes, productivity at the population level was about four times greater at the temperate site, mainly due to the much higher breeding densities compared with Finland. Tengmalm's Owls at the temperate study site may benefit from relatively stable prey abundance, a more diverse prey community that offers alternative prey during vole scarcity, longer nights in summer that allow more time for foraging, and a lower level of interspecific competition with other vole‐specialized predators.     

Collection and cryopreservation of preimplantation embryos of Cavia porcellus

Individual differences and a rather long-lasting reproductive cycle, as well as the relatively small number of oocytes that mature during one reproductive cycle makes it difficult to establish a cryopreserved stock of preimplantation embryos of the guineapig (Cavia porcellus) when compared with other laboratory rodents. Only a few data for superovulation protocols that can be used for routine laboratory use in guineapigs are available. However, a huge number of different strains exist for many purposes and the establishment of a frozen repository makes sense. Here, we describe the successful freezing of preimplatation embryos of the strain 2BS with a two-step freezing protocol in a freezing medium containing 1,2-propanediol as cryoprotectant. Human menopausal gonodotrophin induced superovulation in the embryo donors.     

Short- and long-term effects of litter size manipulation in a small wild-derived rodent

Iteroparous organisms maximize their overall fitness by optimizing their reproductive effort over multiple reproductive events. Hence, changes in reproductive effort are expected to have both short- and long-term consequences on parents and their offspring. In laboratory rodents, manipulation of reproductive efforts during lactation has however revealed few short-term reproductive adjustments, suggesting that female laboratory rodents express maximal rather than optimal levels of reproductive investment as observed in semelparous organisms. Using a litter size manipulation (LSM) experiment in a small wild-derived rodent (the common vole; Microtus arvalis), we show that females altered their reproductive efforts in response to LSM, with females having higher metabolic rates and showing alternative body mass dynamics when rearing an enlarged rather than reduced litter. Those differences in female reproductive effort were nonetheless insufficient to fully match their pups’ energy demand, pups being lighter at weaning in enlarged litters. Interestingly, female reproductive effort changes had long-term consequences, with females that had previously reared an enlarged litter being lighter at the birth of their subsequent litter and producing lower quality pups. We discuss the significance of using wild-derived animals in studies of reproductive effort optimization.     

Evolution of eutherian cytochrome c oxidase subunit II: heterogeneous rates of protein evolution and altered interaction with cytochrome c

Cytochrome c oxidase subunit II (COII), encoded by the mitochondrial genome, exhibits one of the most heterogeneous rates of amino acid replacement among placental mammals. Moreover, it has been demonstrated that cytochrome c oxidase has undergone a structural change in higher primates which has altered its physical interaction with cytochrome c. We collected a large data set of COII sequences from several orders of mammals with emphasis on primates, rodents, and artiodactyls. Using phylogenetic hypotheses based on data independent of the COII gene, we demonstrated that an increased number of amino acid replacements are concentrated among higher primates. Incorporating approximate divergence dates derived from the fossil record, we find that most of the change occurred independently along the New World monkey lineage and in a rapid burst before apes and Old World monkeys diverged. There is some evidence that Old World monkeys have undergone a faster rate of nonsynonymous substitution than have apes. Rates of substitution at four-fold degenerate sites in primates are relatively homogeneous, indicating that the rate heterogeneity is restricted to nondegenerate sites. Excluding the rate acceleration mentioned above, primates, rodents, and artiodactyls have remarkably similar nonsynonymous replacement rates. A different pattern is observed for transversions at four-fold degenerate sites, for which rodents exhibit a higher rate of replacement than do primates and artiodactyls. Finally, we hypothesize specific amino acid replacements which may account for much of the structural difference in cytochrome c oxidase between higher primates and other mammals.      

小型啮齿动物的繁殖能量代价

繁殖是动物向后代传递和保持遗传信息的方式。因此繁殖的意义是显而易见的,但也需要付出代价。主要代价是能量需求增加。在对小家鼠繁殖能量需求的研究中发现,能量摄入在妊娠期只是稍微增加,而在哺乳期则急剧增加。尽管在妊娠期增加的幅度很小,但这可能反映了消化道和发育的胎儿之间在动物腹中的空间竞争,从而可能使能量摄入受到限制进而影响到繁殖过程。哺乳期间,能量摄入急剧增加,在哺乳后期达到高峰并趋于稳定。对野生鼠的研究也表明,野生鼠妊娠期和哺乳期的能量摄入模式与小家鼠是基本相同的,这样我们在小家鼠研究工作中的发现就具有更普遍的适应意义。对哺乳后期能量摄入的限制机制研究至少已经进行了15 年。能量摄入受消化道消化能力的限制(中心限制假说)或者受乳腺泌乳能力限制(外周限制假说) 的假说,都不能合理地解释一些现有的结果。我们提出了一个新的假说,即能量摄入可能受啮齿动物散热能力的限制(热耗散限制假说)。很久以来,一直认为散热能力是对大型哺乳动物哺乳的一个限制因素,但它在小型啮齿动物中的意义尚不清楚。传统观点认为,啮齿动物哺乳期对褐色脂肪组织产热水平的调节是为了重新分配能量以满足哺乳所需;但现在看来,实际上可能是动物为了避免体温过高而降低其基本的产热水平。我们在这个领域已经有了一些进展,但要利用这些知识来理解即使很简单的生活史权衡等问题也还有很多的工作需要做。     

Leptin, but not immune function, is linked to reproductive responsiveness to photoperiod

Energetic demands are high while energy availability is minimum during winter. To cope with this energetic bottleneck, animals exhibit numerous energy-conserving adaptations during winter, including changes in immune and reproductive functions. A majority of individual rodents within a population inhibits reproductive function (responders) as winter approaches. A substantial proportion of small rodents within a species, however, fails to inhibit reproduction (nonresponders) during winter in the field or in the laboratory when maintained in winter-simulated day lengths. In contrast, immune function is bolstered by short day lengths in some species. The specific mechanisms that link reproductive and immune functions remain unspecified. Leptin is a hormone produced by adipose tissue, and several studies suggest that leptin modulates reproductive and immune functions. The present study sought to determine if photoperiodic alterations in reproductive function and leptin concentrations are linked to photoperiod-modulated changes in immune function. Siberian hamsters (Phodopus sungorus) were housed in either long (LD 16:8) or short (LD 8:16) day lengths for 9 wk. After 9 wk, blood samples were collected during the middle of the light and dark phase to assess leptin concentrations. One week later, animals were injected with keyhole limpet hemocyanin to evaluate humoral immunity. Body mass, body fat content, and serum leptin concentrations were correlated with reproductive responsiveness to photoperiod; short-day animals with regressed gonads exhibited a reduction in these measures, whereas short-day nonresponders resembled long-day animals. In contrast, immune function was influenced by photoperiod but not reproductive status. Taken together, these data suggest that humoral immune function in Siberian hamsters is independent of photoperiod-mediated changes in leptin concentrations.     

Reduced anxiety in postpartum rats requires recent physical interactions with pups, but is independent of suckling and peripheral sources of hormones

Changes in emotional behavior occur across the reproductive cycle in female rodents, with reduced anxiety found during the postpartum period, but relatively little is known about factors contributing to this decreased anxiety. Using increased duration of time spent in the open arms of an elevated plus-maze as an indicator of reduced anxiety, it was found in a series of experiments that (1) anxiety is significantly reduced in Long-Evans females during the first week of lactation, but not thereafter, (2) relatively recent contact with pups before testing (within 4 h) is necessary for their reduced anxiety, (3) dams that receive only distal sensory cues from pups for the 4 h prior to testing do not show reduced anxiety, (4) the absence of nipples, and therefore a lack of suckling by pups, has no effect on dams' anxiety, (5) cesarean delivery of pups 2 days prior to expected parturition did not alter later anxiety in dams, (6) hypophysectomy during mid-pregnancy or ovariectomy within 24 h after parturition also did not prevent reduced anxiety in dams, and (7) differences in anxiety between lactating and virgin females are greatest 4-8 min after being placed in the plus-maze. Therefore, exposure to their own peripheral hormones through mid-pregnancy is sufficient to prime female rats to show reduced anxiety, but only if they later have recent physical interaction with pups. Furthermore, because suckling and the peripheral hormones released during suckling appear to be unnecessary, decreased anxiety in maternal rats may instead be regulated by the transient intracerebral release of neuropeptides or neurotransmitters while dams receive other types of tactile inputs from their infants.     

Is the Clavicle of Apes Long? An Investigation of Clavicular Length in Relation to Body Mass and Upper Thoracic Width

An elongated clavicle is one of the distinct features of apes and humans. It plays an important role in providing mobility as well as stability for the shoulder joints. The relative length of the clavicle is an especially important factor in limiting the range of shoulder joint excursion. It is said that among primates, Asian apes, i.e., gibbons and orang-utans, have very long clavicles. At the same time, they also have a wide upper thoracic cage, which may diminish the effective length of the clavicle. To clarify the length of the clavicle in apes, from the standpoint of the functional anatomy of the shoulder girdle, we examined clavicular length in 15 anthropoid species exhibiting various positional behaviors. The results confirm that clavicle length in Asian apes is long, and chimpanzees have a short clavicle like that of Old and New World monkeys, when scaled to body mass. The clavicular length of chimpanzees, however, is intermediate between Old World monkeys and Asian apes when scaled against thoracic width. Therefore, living apes can be grouped together, albeit just barely, by possession of a relatively long clavicle for their thoracic cage size. Interestingly, New World monkeys tend to exhibit a longer clavicle than Old World monkeys of equivalent body mass or thoracic cage width. Although it is unclear whether the ancestral condition of clavicular length in anthropoids was similar to that of living Old or New World monkeys, an elongation of clavicle was an important step toward evolution of the modern body plan of hominoids.