Molecular genetics of Rhabdomys pumilio subspecies boundaries: mtDNA phylogeography and karyotypic analysis by fluorescence in situ hybridization

The phylogeography of the African four-striped mouse, Rhabdomys pumilio, was investigated using complete sequences of the mtDNA cytochrome b gene (1140 bp) and a combination of fluorescence in situ hybridization (FISH) and conventional cytogenetic banding techniques (G- and C-banding). Two cytotypes (2n=46 and 2n=48) were identified by cytogenetic analysis. There is no evidence of diploid number variation within populations, difference in gross chromosome morphology or of subtle interchromosomal rearrangements at levels detected by ZOO-FISH. Analysis of the mtDNA cytochrome b resulted in two major lineages that correspond roughly to the xeric and mesic biotic zones of southern Africa. One mtDNA clade comprises specimens with 2n=48 and the other representatives of two cytotypes (2n=48 and 2n=46). The mean sequence divergence (12%, range 8.3-15.6%) separating the two mtDNA clades is comparable to among-species variation within murid genera suggesting their recognition as distinct species, the prior names for which would be R. dilectus and R. pumilio. Low sequence divergences and the diploid number dichotomy within the mesic lineage support the recognition of two subspecies corresponding to R. d. dilectus (2n=46) and R. d. chakae (2n=48). Our data do not support subspecific delimitation within the nominate, R. pumilio. Molecular dating places cladogenesis of the two putative species at less than five million years, a period characterised by extensive climatic oscillations which are thought to have resulted in habitat fragmentation throughout much of the species range.     

Lipids of the stratum corneum vary with cutaneous water loss among larks along a temperature-moisture gradient

We explored the relationship between lipids of the stratum corneum (SC), the barrier to water-vapor diffusion of the skin, and cutaneous water loss (CWL) of species of free-living larks along a temperature-moisture gradient. Our results showed that free fatty acids, cholesterol, and ceramides were the major constituents of SC in larks from different environments including the Netherlands, a mesic environment; Iran, a semiarid region; and several areas in Saudi Arabia, a hot dry desert. We found that CWL was reduced among larks inhabiting deserts, but our data did not support the hypothesis that birds from desert environments have larger quantities of lipids per unit dry mass of the SC than larks from more mesic environments. Instead, larks in arid environments had a higher proportion of ceramides, especially the more polar fractions 4-6, and a smaller proportion of free fatty acids in their SC, an adjustment that apparently reduced their CWL. Subtle changes in the ratios of lipid classes can apparently alter the movement of water vapor through the skin. We hypothesize that desert birds have higher proportions of ceramides in their SC and lower proportions of free fatty acids because this combination allows the lipid lamellae to exist in a more highly ordered crystalline phase and consequently creates a tighter barrier to water-vapor diffusion.     

Phenotypic plasticity and population differentiation in seeds and seedlings of the grass Anthoxanthum odoratum

Summary Seeds of Anthoxanthum odoratum were transplanted reciprocally between a xeric and a mesic field population that were genetically differentiated in adult traits. In one experiment seeds were reciprocally buried in bags in the soil, in a second experiment seeds were reciprocally sown in small plots. For most traits, site effects were much larger than seed-source effects. Germination, emergence, mortality of buried seed and recruitment were significantly higher at the xeric site than at the mesic site, irrespective of population of origin. Seed dormancy, was significantly higher for seed originating from the mesic than from the xeric population. Seedling recruits originating from the xeric population tended to be larger at both sites. Fecundity of seedling recruits depended on the environment; fecundities of plants growing in the xeric site had more than double the fecundity of plants growing in the mesic site. Phenotypic plasticity rather than population differences determined variation in performance in the seed and seedling stages.     

Intraspecific variation in resistance to desiccation and climatic gradients in the distribution of the bush-dwelling land snail Trochoidea simulata

Resistance to desiccation was examined in six populations of the Israeli bush-dwelling snail Trochoidea simulata , a desert species distributed mainly between the 100–200 mm isohyets.
The present study revealed significant intraspecific differences in resistance to desiccation which are correlated with habitat and climatic gradients within the distribution range of the species. Populations from more arid sites were more resistant to desiccation and heat exposure than those from more mesic areas. However, the population from the Rift Valley (an extremely arid region) was surprisingly poorly resistant. Rates of population water loss under the controlled experimental conditions in the laboratory generally matched the calculated water losses during natural summer aestivation.     

Hydric balance and locomotor performance of an anuran (Rhinella marina) invading the Australian arid zone

Invasive species often encounter environmental conditions well outside those found in their native geographic ranges, and thus provide ideal model systems with which to explore responses to novel abiotic challenges. Within Australia, the invasive cane toad Rhinella marina has colonized areas that are considerably more arid than those found within its native range. Has the colonization of these novel environments been accompanied by shifts in physiology and/or locomotor performance? We measured rates of evaporative water loss, water gain, and effects of desiccation on locomotor performance of cane toads from two invasion fronts: one mesic (the wet‐dry tropics) and one arid (the semi‐desert). The two populations diverged substantially. Contrary to intuition (but consistent with intra‐specific comparisons between other toad populations from mesic vs arid areas), rates of evaporative water loss were lower (not higher) in toads from the mesic population. However, arid‐zone toads gained water more rapidly through their ventral surfaces, and rates of water loss and gain were highly correlated within individual toads from the arid‐zone population. Rates of water exchange in laboratory‐acclimated toads from the semi‐arid zone did not differ from those of free‐ranging conspecifics from the same population, suggesting that divergences between mesic and semi‐arid toads reflect genetic changes that have occurred during the species’ Australian invasion. Mesic and semi‐arid toads showed similar locomotor performance (endurance, distance per hop) when fully hydrated, but locomotor performance declined much more rapidly with desiccation in the mesic toads. Thus, within the short (decades‐long) timespan of the cane toad's Australian invasion, there has been substantial population divergence in the ability to withstand desiccating conditions. If we are to accurately predict the distributions (and hence impacts) of invading organisms, we will need to include adaptation potential in risk assessment schemes.     

Phenotypic selection on leaf water use efficiency and related ecophysiological traits for natural populations of desert sunflowers

Plant water-use efficiency (WUE) is expected to affect plant fitness and thus be under natural selection in arid habitats. Although many natural population studies have assessed plant WUE, only a few related WUE to fitness. The further determination of whether selection on WUE is direct or indirect through functionally related traits has yielded no consistent results. For natural populations of two desert annual sunflowers, Helianthus anomalus and H. deserticola, we used phenotypic selection analysis with vegetative biomass as the proxy for fitness to test (1) whether there was direct and indirect selection on WUE (carbon isotope ratio) and related traits (leaf N, area, succulence) and (2) whether direct selection was consistent with hypothesized drought/dehydration escape and avoidance strategies. There was direct selection for lower WUE in mesic and dry H. anomalus populations, consistent with dehydration escape, even though it is the longer lived of the two species. For mesic H. anomalus, direct selection favored lower WUE and higher N, suggesting that plants may be “wasting water” to increase N delivery via the transpiration stream. For the shorter lived H. deserticola in the direr habitat, there was indirect selection for lower WUE, inconsistent with drought escape. There was also direct selection for higher leaf N, succulence and leaf size. There was no direct selection for higher WUE consistent with dehydration avoidance in either species. Thus, in these natural populations of two desert dune species higher fitness was associated with some combination direct and indirect selection for lower WUE, higher leaf N and larger leaf size. Our understanding of the adaptive value of plant ecophysiological traits will benefit from further consideration of related traits such as leaf nitrogen and more tests in natural populations.     

Ecophysiological studies of sonoran Desert plants

Summary Photosynthetic responses to light and temperature are compared for two genetically related chromosomal races of Machaeranthera gracilis. The ancestral foothills race occurs in cooler, more mesic environments, while the derived desert race occurs in more arid environments. The desert race exhibited greater rates of net photosynthesis at all levels of irradiance than did plants of the foothills race. This enhancement is due primarily to a greater quantum yield and leaf density. High light pretreatment significantly increased the photosynthetic capacity of the desert race, with little or no effect on the foothills race. Furthermore, the leaf density of the desert race was affected proportionately more than the foothills race by light pretreatment. The desert race also possessed higher stomatal and mesophyll conductances to CO₂. Both races exhibited enhanced photosynthetic capacities when grown in a warm thermoperiod (35/25 C), relative to a cool thermoperiod (25/15 C), concomitant with slight increases in leaf density. There was a lack of thermal acclimation for both photosynthesis and respiration of the two races. The greater photosynthetic capactity of the desert race is suggested as an evolutionary modification which could account for invasion into and survival in the sonoran Desert.     

The adjustment of avian metabolic rates and water fluxes to desert environments

We tested the hypothesis that birds in arid environments, where primary productivity is low and surface water is scarce, have reduced energy expenditure and water loss compared with their mesic counterparts. Using both conventional least squares regression and regression based on phylogenetically independent contrasts, we showed that birds from desert habitats have reduced basal and field metabolic rates compared with species from mesic areas. Previous work showed that desert birds have reduced rates of total evaporative water loss when exposed to moderate environmental temperatures in the laboratory. We tested whether reduced rates of total evaporative water loss translate into low field water fluxes. Conventional ANCOVA indicated that desert birds have reduced water fluxes, but an analysis based on phylogenetically independent contrasts did not support this finding, despite the wide array of taxonomic affiliations of species in the data set. We conclude that the high ambient temperatures, the low primary productivity, and the water scarcity in desert environments have selected for or resulted in reduced rates of energy expenditure and evaporative water loss in birds that live in these climes.     

Physiological adjustments to arid and mesic environments in larks (Alaudidae)

Because deserts are characterized by low food availability, high ambient temperature extremes, and absence of drinking water, one might expect that birds that live in these conditions exhibit a lower basal metabolic rate (BMR), reduced total evaporative water loss (TEWL), and greater ability to cope with high air temperatures than their mesic counterparts. To minimize confounding effects of phylogeny, we compared the physiological performance of four species of larks at ambient temperatures (T(a)'s) ranging from 0 degrees to 50 degrees C: hoopoe larks (Alaemon alaudipes) and Dunn's larks (Eremalauda dunni) live in hot and dry deserts, whereas skylarks (Alauda arvensis) and woodlarks (Lullula arborea) occur in temperate mesic areas. Mass-adjusted BMR and TEWL were indistinguishable between hoopoe lark and Dunn's lark and between skylark and woodlark. When grouping the data of the two desert larks in one set and the data of the two mesic larks in another, desert larks are shown to have 43% lower BMR levels and 27% lower TEWL values than the mesic species. Their body temperatures (T(b)'s) were 1.1 degrees C lower, and the minimal dry heat transfer coefficients (h) were 26% below values for the mesic larks. When T(a) exceeded T(b), the h of hoopoe larks and Dunn's larks was high and indistinguishable from h at 40 degrees C, in contrast to the prediction that h should be decreased to minimize heat gain through conductance, convection, or radiation from the environment when T(a) exceeds T(b).     

Axis differentiation in two South American Nothofagus species (Nothofagaceae)

An analysis was carried out on the length, diameter and number of leaves, and the ratios between these variables for current-year growth units (sibling growth units) derived from different nodes of previous-year growth units (parent growth units) of young Nothofagus dombeyi and Nothofagus pumilio trees. Changes in sibling growth unit length, diameter, and number of leaves with position on the parent growth unit were assessed. In both species, sibling-growth unit morphology varied according to both the axis type of the parent growth unit and the position of the sibling growth unit on its parent growth unit. For the largest parent growth units, the length, diameter and number of leaves of their sibling growth units decreased from distal to proximal positions on the parent growth unit. Distal sibling growth units had a more slender stem and longer internodes than proximal sibling growth units. Sibling growth units in equivalent positions tended to have a more slender stem for N. dombeyi than for N. pumilio. Long main-branch growth units of N. pumilio had longer internodes than those of N. dombeyi; the converse was true for shorter growth units. The growth unit diameter/leaf number ratio was consistently higher for N. pumilio than for N. dombeyi. Nothofagus pumilio axes would go through a faster transition from an 'exploring' morphology to an 'exploiting' morphology than N. dombeyi axes. Within- and between-species variations in growth unit morphology should be considered when assessing the adaptive value of the branching pattern of plants.     

Following the rivers: historical reconstruction of California voles Microtus californicus (Rodentia: Cricetidae) in the deserts of eastern California

The California vole, Microtus californicus, restricted to habitat patches where water is available nearly year‐round, is a remnant of the mesic history of the southern Great Basin and Mojave deserts of eastern California. The history of voles in this region is a model for species‐edge population dynamics through periods of climatic change. We sampled voles from the eastern deserts of California and examined variation in the mitochondrial cytb gene, three nuclear intron regions, and across 12 nuclear microsatellite markers. Samples are allocated to two mitochondrial clades: one associated with southern California and the other with central and northern California. The limited mtDNA structure largely recovers the geographical distribution, replicated by both nuclear introns and microsatellites. The most remote population, Microtus californicus scirpensis at Tecopa near Death Valley, was the most distinct. This population shares microsatellite alleles with both mtDNA clades, and both its northern clade nuclear introns and southern clade mtDNA sequences support a hybrid origin for this endangered population. The overall patterns support two major invasions into the desert through an ancient system of riparian corridors along streams and lake margins during the latter part of the Pleistocene followed by local in situ divergence subsequent to late Pleistocene and Holocene drying events. Changes in current water resource use could easily remove California voles from parts of the desert landscape.     

Water balance in desert Drosophila: lessons from non-charismatic microfauna

Water stress is a particularly important problem for insects and other small organisms in arid environments. Cactophilic fruit flies in the genus Drosophila have invaded deserts on numerous occasions, including multiple independent invasions of North American deserts. Because the evolutionary history of this genus is so well studied, we can investigate the mechanisms of adaptation in a rigorous phylogenetic context. As expected, desert fruit flies lose water less rapidly than their mesic congeners. They are also able to tolerate the loss of a greater percentage of body water, but this difference is mainly due to phylogenetic history, and does not represent an adaptation specifically to desert habitats. A laboratory analogue of desert Drosophila is provided by populations of D. melanogaster that have been subjected to selection for desiccation resistance. Selected populations resemble desert species in that they lose water slowly, relative to control populations, and are not more tolerant of dehydration stress. They differ, however, in having much higher water contents and different behavioral responses to desiccating conditions. Our comparisons of laboratory and natural populations reveal that not all possible adaptive mechanisms evolve in stressful environments. Different physiological and behavioral strategies may evolve depending upon the particular options available in the environment.     

Ecological and evolutionary physiology of desert birds: a progress report

The adaptive significance of mechanisms of energy and water conservation among species of desert rodents, which avoid temperature extremes by remaining within a burrow during the day, is well established. Conventional wisdom holds that arid-zone birds, diurnal organisms that endure the brunt of their environment, occupy these desert climates because of the possession of physiological design features common to all within the class Aves. We review studies that show that desert birds may have evolved specific features to deal with hot desert conditions including: a reduced basal metabolic rate (BMR) and field metabolic rate (FMR), and lower total evaporative water loss (TEWL) and water turnover (WTO).Previous work on the comparative physiology of desert birds relied primarily on information gathered on species from the deserts of the southwestern U.S., which are semi-arid habitats of recent geologic origin. We include data on species from Old World deserts, which are geologically older than those in the New World, and place physiological responses along an aridity axis that includes mesic, semi-arid, arid, and hyperarid environments.The physiological differences between desert and mesic birds that we have identified using the comparative method could arise as a result of acclimation to different environments, of genetic change mediated by selection, or both. We present data on the flexibility of BMR and TEWL in Hoopoe Larks that suggest that phenotypic adjustments in these variables can be substantial. Finally, we suggest that linkages between the physiology of individual organism and its life-history are fundamental to the understanding of life-history evolution.     

Cutaneous water loss and the development of the stratum corneum of nestling house sparrows (Passer domesticus) from desert and mesic environments

Evaporation through the skin contributes to more than half of the total water loss in birds. Therefore, we expect the regulation of cutaneous water loss (CWL) to be crucial for birds, especially those that live in deserts, to maintain a normal state of hydration. Previous studies in adult birds showed that modifications of the lipid composition of the stratum corneum (SC), the outer layer of the epidermis, were associated with changes in rates of CWL. However, few studies have examined the ontogeny of CWL and the lipids of the SC in nestling birds. In this study, we measured CWL and the lipid composition of the SC during development of nestlings from two populations of house sparrows, one from the deserts of Saudi Arabia and the other from mesic Ohio. We found that desert and mesic nestlings followed different developmental trajectories for CWL. Desert nestlings seemed to make a more frugal use of water than did mesic nestlings. To regulate CWL, nestlings appeared to modify the lipid composition of the SC during ontogeny. Our results also suggest a tighter regulation of CWL in desert nestlings, presumably as a result of the stronger selection pressures to which nestlings are exposed in deserts.     

Annual plant–shrub interactions along an aridity gradient

Annual plants in semi-arid and arid areas are often closely associated with shrubs. The degree of association largely depends on the balance of negative and positive effects between these contrasting plant life-forms, ranging from interference to facilitation. Since positive interactions are predicted to become less important with increasing rainfall, the interaction balance is expected to shift along aridity gradients. However, this prediction has not been tested on a community level and for different life-history stages across large geographical gradients. Here, we show such changes for annual plant populations and communities in four contrasting sites along a steep climatic gradient, ranging from the arid desert to mesic Mediterranean regions in Israel. Above-ground productivity, richness, seedling density, and seed bank density of the annual plant community, as well as fecundity of annual plant populations, were generally higher under shrubs than in areas between shrubs at the arid end of the gradient, but significantly lower at the humid end. Net effects of shrubs on annuals expressed as relative interaction intensity indicated a steady and consistent shift from net positive or neutral effects in the desert to net negative effects in the mesic part of the gradient. These findings emphasize the usefulness of studies along large-scale gradients encompassing a wide range of environmental conditions for understanding community level interactions among coexisting species.     

Discontinuous ventilation and energetics of locomotion in the desert-dwelling female mutillid wasp, Dasymutilla gloriosa

Abstract. Data on the discontinuous ventilation cycle and cost of pedestrian locomotion in female Dasymutilla gloriosa (Sauss.), a desert-dwelling mutillid, are described and compared with equivalent data from other Hymenoptera. The discontinuous ventilation cycle was intermediate between that found in xeric and mesic hymenopterans, with the open phase being about 20% of the cycle. No noticeable flutter phase was observed. Thus D. gloriosa does not attempt to reduce respiratory water loss to the same extent as found in other desert dwelling Hymenoptera. The minimum cost of transport was significantly higher than that obtained for several ant species, indicating that ants are probably more efficient runners than any other Hymenoptera.     

Seasonal abundance patterns of the sandfly Phlebotomus papatasi in climatically distinct foci of cutaneous leishmaniasis in Israeli deserts

Among foci of cutaneous leishmaniasis in Israel, population densities of the vector sandfly Phlebotomus papatasi Scopoli (Diptera: Psychodidae) were assessed during April-October 1999 in the mesic Negev desert and the hyper-xeric Arava valley, using sticky traps placed overnight near host burrows of the fat sand rat, Psammomys obesus Cretzschmar (Cricetidae: Gerbillinae). Population dynamics of Ph. papatasi differed between the Negev (study sites on sand near Mount Keren and on loess at Nizzana ruins) and the Arava valley (study sites on sand at Shezaf and in a fallow field near irrigation at wadi Arava). At the Negev sites, sandfly abundance peaked in spring (April or May), whereas at Arava sites Ph. papatasi population densities were bi-modal, with peaks in both spring and autumn (September or October). This might be conducive to sustaining enzootic Leishmania major Yakimoff & Schokhor (Kinetoplastida: Trypanosomatidae). In both areas, Ph. papatasi densities were much higher at the site with moister soil, raising transmission risks of zoonotic cutaneous leishmaniasis.     

The role of climate,water and biotic interactions in shaping biodiversity patterns in arid environments across spatial scales

Aim

Desert ecosystems, with their harsh environmental conditions, hold the key to understanding the responses of biodiversity to climate change. As desert community structure is influenced by processes acting at different spatial scales, studies combining multiple scales are essential for understanding the conservation requirements of desert biota. We investigated the role of environmental variables and biotic interactions in shaping broad and fine‐scale patterns of diversity and distribution of bats in arid environments to understand how the expansion of nondesert species can affect the long‐term conservation of desert biodiversity.

Location

Levant, Eastern Mediterranean.

Methods

We combine species distribution modelling and niche overlap statistics with a statistical model selection approach to integrate interspecific interactions into broadscale distribution models and fine‐scale analysis of ecological requirements. We focus on competition between desert bats and mesic species that recently expanded their distribution into arid environment following anthropogenic land‐use changes.

Results

We show that both climate and water availability limit bat distributions and diversity across spatial scales. The broadscale distribution of bats was determined by proximity to water and high temperatures, although the latter did not affect the distribution of mesic species. At the fine‐scale, high levels of bat activity and diversity were associated with increased water availability and warmer periods. Desert species were strongly associated with warmer and drier desert types. Range and niche overlap were high among potential competitors, but coexistence was facilitated through fine‐scale spatial partitioning of water resources.

Main conclusions

Adaptations to drier and warmer conditions allow desert‐obligate species to prevail in more arid environments. However, this competitive advantage may disappear as anthropogenic activities encroach further into desert habitats. We conclude that reduced water availability in arid environments under future climate change projections pose a major threat to desert wildlife because it can affect survival and reproductive success and may increase competition over remaining water resources.     

Molecular genetics of Rhabdomys pumilio subspecies boundaries: mtDNA phylogeography and karyotypic analysis by fluorescence in situ hybridization

The phylogeography of the African four-striped mouse, Rhabdomys pumilio, was investigated using complete sequences of the mtDNA cytochrome b gene (1140 bp) and a combination of fluorescence in situ hybridization (FISH) and conventional cytogenetic banding techniques (G- and C-banding). Two cytotypes (2n=46 and 2n=48) were identified by cytogenetic analysis. There is no evidence of diploid number variation within populations, difference in gross chromosome morphology or of subtle interchromosomal rearrangements at levels detected by ZOO-FISH. Analysis of the mtDNA cytochrome b resulted in two major lineages that correspond roughly to the xeric and mesic biotic zones of southern Africa. One mtDNA clade comprises specimens with 2n=48 and the other representatives of two cytotypes (2n=48 and 2n=46). The mean sequence divergence (12%, range 8.3–15.6%) separating the two mtDNA clades is comparable to among-species variation within murid genera suggesting their recognition as distinct species, the prior names for which would be R. dilectus and R. pumilio. Low sequence divergences and the diploid number dichotomy within the mesic lineage support the recognition of two subspecies corresponding to R. d. dilectus (2n=46) and R. d. chakae (2n=48). Our data do not support subspecific delimitation within the nominate, R. pumilio. Molecular dating places cladogenesis of the two putative species at less than five million years, a period characterised by extensive climatic oscillations which are thought to have resulted in habitat fragmentation throughout much of the species range.