Evolution of the spermatozoon in muroid rodents

In the rodent superfamily Muroidea, a model for the evolution of sperm form has been proposed in which it is suggested that a hook-shaped sperm head and long tail evolved from a more simple, nonhooked head and short tail in several different subfamilies. To test this model the shape of the sperm head, with particular emphasis on its apical region, and length of sperm tail were matched to a recent phylogeny based on the nucleotide sequence of several protein-coding nuclear genes from 3 families and 10 subfamilies of muroid rodents. Data from the two other myomorph superfamilies, the Dipodoidea and kangaroo rats in the Geomyoidea, were used for an outgroup comparison. In most species in all 10 muroid subfamilies, apart from in the Murinae, the sperm head has a long rostral hook largely composed of acrosomal material, although its length and cross-sectional shape vary across the various subfamilies. Nevertheless, in a few species of various lineages a very different sperm morphology occurs in which an apical hook is lacking. In the outgroups the three species of dipodid rodents have a sperm head that lacks a hook, whereas in the heteromyids an acrosome-containing apical hook is present. It is concluded that, as the hook-shaped sperm head and long sperm tail occur across the muroid subfamilies, as well as in the heteromyid rodents, it is likely to be the ancestral condition within each of the subfamilies with the various forms of nonhooked sperm heads, that are sometimes associated with short tails, being highly derived states. These findings thus argue against a repeated evolution in various muroid lineages of a complex, hook-shaped sperm head and long sperm tail from a more simple, nonhooked sperm head and short tail. An alternative proposal for the evolution of sperm form within the Muroidea is presented in the light of these data.     

Pregnancy initiation in postpartum estrus in three species of muroid rodents.

Pregnancy initiation in postpartum estrus was studied in 14 male-female pairs of white-footed mice, Peromyscus leucopus; 12 pairs of prairie voles, Microtus ochrogaster; and 14 pairs of montane voles, M. montanus. When mated for one ejaculatory series, the percentages of females pregnant were 25, 43, and 71% for M. ochrogaster, M. montanus, and P. leucopus, respectively. Whereas mating to satiety produced a significant increase in the probability of pregnancy relative to mating for one ejaculatory series in M. montanus, there was no significant difference in P. leucopus. M. ochrogaster did not differ significantly when mated for one ejaculation versus two. P. leucopus resemble P. maniculatus in having a lower stimulus requirement for pregnancy initiation in postpartum than in cycling estrus. M. ochrogaster resemble laboratory rats in having a higher stimulus requirement for pregnancy initiation in postpartum estrus. M. montanus show no significant difference.     

Effects of vaginal-cervical stimulation in seven species of muroid rodents.

Six species of muroid rodents (Peromyscus californicus, P. eremicus, P. gossypinus, Mesocricetus auratus, Rattus norvegicus and R. rattus) were given artificlal vaginal-cervical stimulation in an attempt to induce pseudopregnancy. Some females of each species became pseudopregnant, but it was not clear that stimulation patterns mimicking the copulatory patterns of conspecific males were more effective than other patterns of stimulation. In the non-domesticated species (Peromyscus and R. rattus) a few females responded to a variety of stimulus conditions, and no species differences in responsiveness among the wild species were evident. The established laboratory rodents (R. norvegicus, M. auratusy were markedly more responsive to artificial stimulation, suggesting possible effects of domestication on fecundity and reactions to handling- Microtus ochrogaster, an induced ovulator, ovulated in response to vaginal-cervical stimulation only if one intromission from a male was also provided. No other differences in the responses of reflex and spontaneous ovulators were apparent.     

Ecomorphological diversification following continental colonization in muroid rodents (Rodentia: Muroidea)

The emergence of exceptionally diverse clades is often attributed to ecological opportunity. For example, the exceptional diversity in the most diverse superfamily of mammals, muroid rodents, has been explained in terms of multiple independent adaptive radiations. If multiple ecological opportunity events are responsible for generating muroid diversity, we expect to find evidence of these lineages ecologically diversifying following dispersal into new biogeographical areas. In the present study, we tested the trait‐based predictions of ecological opportunity using data on body size, appendages, and elevation in combination with previously published data on biogeographical transitions and a time‐calibrated molecular phylogeny. We identified weak to no support of early ecological diversification following the initial colonizations of all continental regions, based on multiple tests, including node height tests, disparity through time plots, evolutionary model comparison, and Bayesian analysis of macroevolutionary mixtures. Clades identified with increased diversification rates, not associated with geographical transitions, also did not show patterns of phenotypic divergence predicted by ecological opportunity, which suggests that phylogenetic diversity and phenotypic disparity may be decoupled in muroids. These results indicate that shifts in diversification rates and biogeographically‐mediated ecological opportunity are poor predictors of phenotypic diversity patterns in muroids.     

Retrofitting the genome: L1 extinction follows endogenous retroviral expansion in a group of muroid rodents

Long interspersed nuclear element 1 (LINE-1; L1) retrotransposons are the most common retroelements in mammalian genomes. Unlike individual families of endogenous retroviruses (ERVs), they have remained active throughout the mammalian radiation and are responsible for most of the retroelement movement and much genome rearrangement within mammals. They can be viewed as occupying a substantial niche within mammalian genomes. Our previous demonstration that L1s and B1 short interspersed nuclear elements (SINEs) are inactive in a group of South American rodents led us to ask if other elements have amplified to fill the empty niche. We identified a novel and highly active family of ERVs (mysTR). To determine whether loss of L1 activity was correlated with expansion of mysTR, we examined mysTR activity in four South American rodent species that have lost L1 and B1 activity and four sister species with active L1s. The copy number of recent mysTR insertions was extremely high, with an average of 4,200 copies per genome. High copy numbers exist in both L1-active and L1-extinct species, so the mysTR expansion appears to have preceded the loss of both SINE and L1 activity rather than to have filled an empty niche created by their loss. It may be coincidental that two unusual genomic events--loss of L1 activity and massive expansion of an ERV family--occur in the same group of mammals. Alternatively, it is possible that this large ERV expansion set the stage for L1 extinction.     

Evolutionary history of the most speciose mammals: molecular phylogeny of muroid rodents

Phylogenetic relationships between 32 species of rodents representing 14 subfamilies of Muridae and four subfamilies of Dipodidae were studied using sequences of the nuclear protein-coding genes Lecithin Cholesterol Acyl Transferase (LCAT) and von Willebrand Factor (vWF). An examination of some evolutionary properties of each data matrix indicates that the two genes are rather complementary, with lower rates of nonsynonymous substitutions for LCAT. Both markers exhibit a wide range of GC3 percentages (55%-89%), with several taxa above 70% GC3 for vWF, which indicates that those exonic regions might belong to the richest class of isochores. The primary sequence data apparently harbor few saturations, except for transitions on third codon positions for vWF, as indicated by comparisons of observed and expected pairwise values of substitutions. Phylogenetic trees based on 1,962 nucleotidic sites from the two genes indicate that the 14 Muridae subfamilies are organized into five major lineages. An early isolation leads to the clade uniting the fossorial Spalacinae and semifossorial Rhizomyinae with a strong robustness. The second lineage includes a series of African taxa representing nesomyines, dendromurines, cricetomyines, and the sole living member of mystromyines. The third one comprises only the mouselike hamster CALOMYSCUS: The fourth clade represents the cricetines, myospalacines, sigmodontines, and arvicolines, whereas the fifth one comprises four "traditional" subfamilies (Gerbillinae, Murinae, Otomyinae, and Acomyinae). Within these groups, we confirm the monophyly of almost all studied subfamilies, namely, Spalacinae, Rhizomyinae, Nesomyinae, Cricetomyinae, Arvicolinae, Sigmodontinae, Cricetinae, Gerbillinae, Acomyinae, and Murinae. Finally, we present evidence that the sister group of Acomyinae is Gerbillinae, and we confirm a nested position of Myospalacinae within Cricetinae and Otomyinae within Murinae. From a biogeographical point of view, the five main lineages spread and radiated from Asia with different degrees of success: the first three groups are now represented by a limited number of species and genera localized in some regions, whereas the last two groups radiated in a large variety of species and genera dispersed all over the world.     

The comparative gastrointestinal morphology of five species of muroid rodents found in Saudi Arabia

Meriones rex (King jird), Meriones libycus (Libyan jird), Acomys dimidiatus (Eastern spiny mouse), Acomys cahirinus (Egyptian spiny mouse), and Dipodillus dasyurus (Wagner's dipodil) are five species of small rodents of the superfamily Muroidea with distributions in Eastern Africa, Egypt, and the desert regions of the Arabian Peninsula. Water is scarce in these regions and may result in relatively low‐digestible food. The aim of the present study is to describe and compare the gastrointestinal tract morphology and morphometry of these five species in order to elucidate whether morphology is influenced by phylogeny or dietary preference. Each segment of the gastrointestinal tract of each species was macroscopically examined and the length and basal surface area of each segment was measured. Standard histologic procedures were performed to determine a surface enlargement factor to determine the mucosal luminal surface area. A unilocular‐hemiglandular stomach was observed in all the species examined. The caeca of all the species were long and arranged into a loose spiral toward the caecal tip with the ileocaecal and caeco‐colic openings positioned close together. Two rows of oblique folds could be observed in the proximal colon of all species except in D. dasyurus which had longitudinal folds. Morphometric analysis showed the largest stomach in A. cahirinus and the largest caecum and colon in M. libycus. All the species can be grouped in the family Muridae in two subfamilies and similarities were observed including the hemiglandular stomach and relatively large caecum. It could be concluded that phylogeny plays an important role in determining gastrointestinal morphology while diet plays a subordinate role in the desert rodents in the present study. J. Morphol. 275:980–990, 2014. © 2014 Wiley Periodicals, Inc.     

Concentration and size distribution of plant fiber in the digestive tract of muroid rodents

The weight parameters that characterize the size and the degree of fullness of fermentation chambers (forestomach and cecum), namely, the weight of the walls and the content of these organs, and the concentration and size distribution of fibers in the chyme have been investigated in five muroid rodent species (Arvicola terrestris, Microtus oeconomus, Microtus arvalis sp., Clethrionomys glareolus, and Sylvaemus flavicollis). No distinct regularities were observed in the above-mentioned parameters of the forestomach. These parameters of the cecum were generally found to be in good agreement with the conventional concept of dietary specialization of the rodent species under investigation, but the results have provided a more precise assessment of the role of dietary fiber in the diet of free-living rodents under specific environmental conditions.     

Phylogeny of muroid rodents: relationships within and among major lineages as determined by IRBP gene sequences

The rodent family Muridae is the single most diverse family of mammals with over 1300 recognized species. We used DNA sequences from the first exon ( approximately 1200bp) of the IRBP gene to infer phylogenetic relationships within and among the major lineages of muroid rodents. We included sequences from every recognized muroid subfamily except Platacanthomyinae and from all genera within the endemic Malagasy subfamily Nesomyinae, all recognized tribes of Sigmodontinae, and a broad sample of genera in Murinae. Phylogenetic analysis of the IRBP data suggest that muroid rodents can be sorted into five major lineages: (1) a basal clade containing the fossorial rodents in the subfamilies Spalacinae, Myospalacinae, and Rhizomyinae, (2) a clade of African and Malagasy genera comprising the subfamilies Petromyscinae, Mystromyinae, Cricetomyinae, Nesomyinae, and core dendromurines, (3) a clade of Old World taxa belonging to Murinae, Otomyinae, Gerbillinae, Acomyinae, and Lophiomyinae, (4) a clade uniting the subfamilies Sigmodontinae, Arvicolinae, and Cricetinae, and (5) a unique lineage containing the monotypic Calomyscinae. Although relationships among the latter four clades cannot be resolved, several well-supported supergeneric groupings within each are identified. A preliminary examination of molar tooth morphology on the resulting phylogeny suggests the triserial murid molar pattern as conceived by evolved at least three times during the course of muroid evolution.     

Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes

The muroid rodents are the largest superfamily of mammals, containing nearly one third of all mammal species. We report on a phylogenetic study comprising 53 genera sequenced for four nuclear genes, GHR, BRCA1, RAG1, and c-myc, totaling up to 6400 nucleotides. Most relationships among the subfamilies are resolved. All four genes yield nearly identical phylogenies, differing only in five key regions, four of which may represent particularly rapid radiations. Support is very strong for a fundamental division of the mole rats of the subfamilies Spalacinae and Rhizomyinae from all other muroids. Among the other "core" muroids, a rapid radiation led to at least four distinct lineages: Asian Calomyscus, an African clade of at least four endemic subfamilies, including the diverse Nesomyinae of Madagascar, a hamster clade with maximum diversity in the New World, and an Old World clade including gerbils and the diverse Old World mice and rats (Murinae). The Deomyinae, recently removed from the Murinae, is well supported as the sister group to the gerbils (Gerbillinae). Four key regions appear to represent rapid radiations and, despite a large amount of sequence data, remain poorly resolved: the base of the "core" muroids, among the five cricetid (hamster) subfamilies, within a large clade of Sigmodontinae endemic to South America, and among major geographic lineages of Old World Murinae. Because of the detailed taxon sampling within the Murinae, we are able to refine the fossil calibration of a rate-smoothed molecular clock and apply this clock to date key events in muroid evolution. We calculate rate differences among the gene regions and relate those differences to relative contribution of each gene to the support for various nodes. The among-gene variance in support is greatest for the shortest branches. We present a revised classification for this largest but most unsettled mammalian superfamily.     

Making pore choices: repeated regime shifts in stomatal ratio

Ecologically important traits do not evolve without limits. Instead, evolution is constrained by the set of available and viable phenotypes. In particular, natural selection may only favour a narrow range of adaptive optima constrained within selective regimes. Here, I integrate data with theory to test whether selection explains phenotypic constraint. A global database of 599 plant species from 94 families shows that stomatal ratio, a trait affecting photosynthesis and defence against pathogens, is highly constrained. Most plants have their stomata on the lower leaf surface (hypostomy), but species with half their stomata on each surface (amphistomy) form a distinct mode in the trait distribution. A model based on a trade-off between maximizing photosynthesis and a fitness cost of upper stomata predicts a limited number of adaptive solutions, leading to a multimodal trait distribution. Phylogenetic comparisons show that amphistomy is the most common among fast-growing species, supporting the view that CO₂ diffusion is under strong selection. These results indicate that selective optima stay within a relatively stable set of selective regimes over macroevolutionary time.     

Heterochronic shifts in germband movements contribute to the rapid embryonic development of the coffin fly Megaselia scalaris

The coffin fly, Megaselia scalaris, is a species of medical and forensic importance and is increasingly being used for the study of genetics. Postmortem interval can be estimated based on the life stage of M. scalaris recovered from corpses, therefore many studies have addressed the duration of each life stage. These studies demonstrate that embryogenesis completes significantly faster in M. scalaris than in the congener Megaselia abdita and faster even than the 24 h needed for Drosophila melanogaster embryogenesis. However, until now it has been unclear if this increased speed is achieved by reducing developmental time across all embryonic stages or by the acceleration of individual stages and processes. Here I use time-lapse imaging to create a staging scheme for M. scalaris embryogenesis. Comparison of stages between D. melanogaster and both Megaselia species reveals that heterochronic shifts, simultaneous morphogenetic movements and compression of individual stages all contribute to the rapid development of M. scalaris.     

Soil microbial community shifts explain habitat heterogeneity in two Haloxylon species from a nutrient perspective

Haloxylon ammodendron and Haloxylon persicum (as sister taxa) are dominant shrubs in the Gurbantunggut Desert. The former grows in inter-dune lowlands while the latter in sand dunes. However, little information is available regarding the possible role of soil microorganisms in the habitat heterogeneity in the two Haloxylon species from a nutrient perspective. Rhizosphere is the interface of plant–microbe–soil interactions and fertile islands usually occur around the roots of desert shrubs. Given this, we applied quantitative real-time PCR combined with MiSeq amplicon sequencing to compare their rhizosphere effects on microbial abundance and community structures at three soil depths (0–20, 20–40, and 40–60 cm). The rhizosphere effects on microbial activity (respiration) and soil properties had also been estimated. The rhizospheres of both shrubs exerted significant positive effects on microbial activity and abundance (e.g., eukarya, bacteria, and nitrogen-fixing microbes). The rhizosphere effect of H. ammodendron on microbial activity and abundance of bacteria and nitrogen-fixing microbes was greater than that of H. persicum. However, the fertile island effect of H. ammodendron was weaker than that of H. persicum. Moreover, there existed distinct differences in microbial community structure between the two rhizosphere soils. Soil available nitrogen, especially nitrate nitrogen, was shown to be a driver of microbial community differentiation among rhizosphere and non-rhizosphere soils in the desert. In general, the rhizosphere of H. ammodendron recruited more copiotrophs (e.g., Firmicutes, Bacteroidetes, and Proteobacteria), nitrogen-fixing microbes and ammonia-oxidizing bacteria, and with stronger microbial activities. This helps it maintain a competitive advantage in relatively nutrient-rich lowlands. Haloxylon persicum relied more on fungi, actinomycetes, archaea (including ammonia-oxidizing archaea), and eukarya, with higher nutrient use efficiency, which help it adapt to the harsher dune crests. This study provides insights into the microbial mechanisms of habitat heterogeneity in two Haloxylon species in the poor desert soil.     

Evaluation of alternative hypotheses to explain temperature-induced life history shifts in Daphnia

Negative correlations between environmental temperature andbody size are widespread in planktonic organisms, and ectothermsgenerally, but remain poorly understood. Here we evaluate experimentallytwo alternative hypotheses suggested to explain life historyshifts induced by raised temperature using parthenogenetic clonesfrom two Daphnia species. Explanation 1 proposes that the lifehistory shifts could be adaptive if increased temperature isused as an indirect cue to indicate increased risk from size-selectivepredators. Explanation 2 proposes that at larger body size energybecomes more limiting as temperature increases because of aless favourable assimilation: metabolism balance. In a factoriallaboratory experiment we examine the effects of three rearingtemperatures on the growth and reproductive traits of Daphniaraised in water with fish kairomone, Chaoborus kairomone, orin uncontaminated water. None of the three predictions of explanation1 were met by the data. In both D. pulex and D. curvirostris,and some other published studies, data suggested that at largerbody sizes the sum of growth and reproduction was lower at hightemperature, supporting our prediction from explanation 2. However,we propose a novel third explanation based on new evidence oftemperature-dependence in both reproductive effort and costin D. pulex.     

Heterochronic shifts in the ossification sequences of surface- and subsurface-dwelling skinks are correlated with the degree of limb reduction

Scincid lizards exhibit a variety of limb anatomies which reflect the functional requirements of different modes of life. Besides surface dwellers which show neither body elongation nor limb reduction, there are numerous examples that can be arranged as increasingly serpentiform taxa moving in sand, humus or leaf litter. We explored the question of whether limb reduction and body elongation in skinks are linked to heterochronic shifts in the ossification sequences. The study material comprises skinks showing four different morphotypes: Liopholis whitii, Lerista bougainvillii, Hemiergis peronii and Saiphos equalis. Results showed that (i) scincid lizards with limb reductions exhibit an earlier onset of ossification in the cervical vertebrae, and (ii) ossification starts earlier in the pectoral girdle (scapula and coracoid) and pelvic girdle (ilium, ischium and pubis) relative to the timing of the onset in elements of the forelimbs and hind limbs. Furthermore, they show (iii) an earlier strengthening of the premaxilla, which first completes the anterior part of the dorsal cranial roof, and (iv) an earlier onset of ossification in the forelimb elements than in the equivalent elements of the hind limbs. The species showing the least limb reduction (L. bougainvillii) had the greatest developmental similarity to the normally proportioned surface-dwelling species (L. whitii). S. equalis, as the morphotype with the greatest deviation from the normally proportioned, pentadactyle form, varies the most from L. whitii. The heterochronic shifts in the ossification sequences are linked to a shift in the emphasis from limbed locomotion to trunk locomotion in the species with body elongation and/or limb reduction.     

Environment predicts repeated body size shifts in a recent radiation of Australian mammals*

Closely related species that occur across steep environmental gradients often display clear body size differences, and examining this pattern is crucial to understanding how environmental variation shapes diversity. Australian endemic rodents in the Pseudomys Division (Muridae: Murinae) have repeatedly colonized the arid, monsoon, and mesic biomes over the last 5 million years. Using occurrence records, body mass data, and Bayesian phylogenetic models, we test whether body mass of 31 species in the Pseudomys Division can be predicted by their biome association. We also model the effect of eight environmental variables on body mass. Despite high phylogenetic signal in body mass evolution across the phylogeny, we find that mass predictably increases in the mesic biome and decreases in arid and monsoon biomes. As per Bergmann's rule, temperature is strongly correlated with body mass, as well as several other variables. Our results highlight two important findings. First, body size in Australian rodents has tracked with climate through the Pleistocene, likely due to several environmental variables rather than a single factor. Second, support for both Brownian motion and predictable change at different taxonomic levels in the Pseudomys Division phylogeny demonstrates how the level at which we test hypotheses can alter interpretation of evolutionary processes.     

Gradients in density variations of small rodents: the importance of latitude and snow cover

Summary Microtine rodents are known to show extreme population variations (cycles) but non-cyclic populations have also been recognized during recent years. The cyclic populations have been widely thought to be regulated by intrinsic mechanisms. However, such predictions for cyclic populations are usually not applicable to non-cyclic ones and extrinsic factors may have to be included in any explanation.A hypothesis that the degree of fluctuations in small rodent numbers is related to the sustainable number of generalist predators was tested on mainly literature data by computing indices of cyclicity for local populations. These indices were related to latitude and snow cover (two measures) as these variables will affect the amount of alternative prey available for these generalists. Within Fennoscandia such indices for Clethrionomys glareolus and Microtus agrestis were clearly positively related to latitude and snow cover. The fraction of populations with summer declines in numbers, characterizing highly cyclic populations, increased in the same way. Cyclicity indices in Great Britain were similar to those in southern Fennoscandia, both areas being poor in snow, but were higher at the same latitudes in eastern Europe with more snow. Indices of density variations were generally low in North American Clethrionomys species and very variable in Microtus species.The gradients observed and differences between continents are interpreted as due to microtine-vegetation interactions in northern European areas poor in generalist predators but with important small mustelid predation, and to similar snowshoe hare-vegetation interactions in mainly Canada-Alaska, where small rodents may serve as alternative prey for numerically fluctuating hare predators, at least in the forests. Western European microtine populations, and probably many others, seem to be regulated by generalist predators.