Habitat selection as a mechanism of resource partitioning in two cryptic bat species Pipistrellus pipistrellus and Pipistrellus pygmaeus

Ecomorphological studies of bat communities often reveal the spatial and temporal coexistence of morphologically similar species, leading to suggestions that these communities are structured by non-deterministic processes. However, the diversification of echolocation call structure in bats allows for considerable morphological similarity while still permitting niche differentiation based on specialisation for prey type and habitat structure. The recent separation of a common Palaearctic bat, the pipistrelle, into Pipistrellus pipistrellus and P. pygmaeus, which are sympatrically distributed throughout their range, raises the question as to whether these two morphologically similar species partition resources in time and space.
To test the hypothesis that the coexistence of these cryptic species is facilitated by differential habitat use, 14 P . pipistrellus , and 12 P. pygmaeus were radio-tracked from adjacent maternity roosts, in northeast Scotland, from May to September 2002/2003. The two species showed distinct habitat partitioning with P. pygmaeus foraging predominantly in riparian woodland and over water, and P. pipistrellus foraging along woodland edges and short isolated tree lines. Inter-specific overlap in habitat use was low and consequently foraging ranges were segregated spatially.
The degree of habitat partitioning revealed in these species, which show considerable overlap in echolocation call parameters and functional morphology, suggests that morphological features, whilst useful in separating chiropteran species into coarse-grained foraging guilds, may not predict fine-grained ecological segregation.     

The inheritance of mating songs in two cryptic,sibling lacewing species (Neuroptera: Chrysopidae: Chrysoperla)

Speciation often involves incremental responses to natural selection and results in large scale genomic changes, but it may also occur abruptly and with little genetic imprint, as seen in some complexes of cryptic species. Recent attention has focused on sexual selection in rapid speciation, because it can disrupt premating signals that mediate reproductive isolation. Some models require that environmental adaptation assist sexual selection during speciation, while others show that populations can diverge through mate choice alone. We propose that speciation involving environmental adaptation in premating signals is likely to have a polygenic basis, while speciation due to arbitrary changes in premating signals could be accompanied by changes at just a few loci. The sibling species Chrysoperla plorabunda and Chrysoperla johnsoni belong to a large complex of cryptic species of green lacewings, and meet all criteria for speciation via sexual selection. We perform a genetic analysis of line crosses between them, focusing on their substrate-borne premating songs. Measurements of seven song features and their principal components are compared among parentals, F₁ and F₂ hybrids, and backcrosses. The distributions of phenotypes are consistent with a model of more than one, but not many, genes. Sex linkage and/or maternal effects are negligible. C. plorabunda is dominant for most traits affecting mate choice. Bayesian analyses of segregation variance show significant additive and epistatic effects on line means. A Bayesian Castle–Wright estimate suggests that relatively few effective factors are responsible for variation in volley period ( ), number of volleys per song ( ), and PC-1 ( ). Our results are consistent with simple genetic architecture of songs, supporting a role for major genes in premating isolation and strengthening the notion that mate choice alone, without significant environmental adaptation, has been responsible for generating new lacewing species.     

Mitogenomics reveals two cryptic species in Ciona intestinalis

Individual mitochondrial genes or genomic features are commonly used as phylogenetic markers at many taxonomic levels. We used a mitogenomics approach to demonstrate the existence of two cryptic species in the ascidian Ciona intestinalis, a model chordate whose status as a single species has recently been questioned. Comprehensive comparative analysis of the mitochondrial genome of the two cryptic species revealed significant differences in gene order, size and number of noncoding regions, compositional features and divergence of protein-coding genes.     

High-throughput sequencing offers insight into mechanisms of resource partitioning in cryptic bat species

Sympatric cryptic species, characterized by low morphological differentiation, pose a challenge to understanding the role of interspecific competition in structuring ecological communities. We used traditional (morphological) and novel molecular methods of diet analysis to study the diet of two cryptic bat species that are sympatric in southern England (Plecotus austriacus and P. auritus) (Fig. 1). Using Roche FLX 454 (Roche, Basel, CH) high-throughput sequencing (HTS) and uniquely tagged generic arthropod primers, we identified 142 prey Molecular Operational Taxonomic Units (MOTUs) in the diet of the cryptic bats, 60% of which were assigned to a likely species or genus. The findings from the molecular study supported the results of microscopic analyses in showing that the diets of both species were dominated by lepidopterans. However, HTS provided a sufficiently high resolution of prey identification to determine fine-scale differences in resource use. Although both bat species appeared to have a generalist diet, eared-moths from the family Noctuidae were the main prey consumed. Interspecific niche overlap was greater than expected by chance (O(jk) = 0.72, P < 0.001) due to overlap in the consumption of the more common prey species. Yet, habitat associations of nongeneralist prey species found in the diets corresponded to those of their respective bat predator (grasslands for P. austriacus, and woodland for P. auritus). Overlap in common dietary resource use combined with differential specialist prey habitat associations suggests that habitat partitioning is the primary mechanism of coexistence. The performance of HTS is discussed in relation to previous methods of molecular and morphological diet analysis. By enabling species-level identification of dietary components, the application of DNA sequencing to diet analysis allows a more comprehensive comparison of the diet of sympatric cryptic species, and therefore can be an important tool for determining fine-scale mechanisms of coexistence.     

Vertical niche partitioning between cryptic sibling species of a cosmopolitan marine planktonic protist

A large portion of the surface‐ocean biomass is represented by microscopic unicellular plankton. These organisms are functionally and morphologically diverse, but it remains unclear how their diversity is generated. Species of marine microplankton are widely distributed because of passive transport and lack of barriers in the ocean. How does speciation occur in a system with a seemingly unlimited dispersal potential? Recent studies using planktonic foraminifera as a model showed that even among the cryptic genetic diversity within morphological species, many genetic types are cosmopolitan, lending limited support for speciation by geographical isolation. Here we show that the current two‐dimensional view on the biogeography and potential speciation mechanisms in the microplankton may be misleading. By depth‐stratified sampling, we present evidence that sibling genetic types in a cosmopolitan species of marine microplankton, the planktonic foraminifer Hastigerina pelagica, are consistently separated by depth throughout their global range. Such strong separation between genetically closely related and morphologically inseparable genetic types indicates that niche partitioning in marine heterotrophic microplankton can be maintained in the vertical dimension on a global scale. These observations indicate that speciation along depth (depth‐parapatric speciation) can occur in vertically structured microplankton populations, facilitating diversification without the need for spatial isolation.     

Reproductive protein evolution in two cryptic species of marine chordate

Background  

Reproductive character displacement (RCD) is a common and taxonomically widespread pattern. In marine broadcast spawning organisms, behavioral and mechanical isolation are absent and prezygotic barriers between species often operate only during the fertilization process. Such barriers are usually a consequence of differences in the way in which sperm and egg proteins interact, so RCD can be manifest as faster evolution of these proteins between species in sympatry than allopatry. Rapid evolution of these proteins often appears to be a consequence of positive (directional) selection. Here, we identify a set of candidate gamete recognition proteins (GRPs) in the ascidian Ciona intestinalis and showed that these GRPs evolve more rapidly than control proteins (those not involved in gamete recognition). Choosing a subset of these gamete recognition proteins that show evidence of positive selection (CIPRO37.40.1, CIPRO60.5.1, CIPRO100.7.1), we then directly test the RCD hypothesis by comparing divergence (omega) and polymorphism (McDonald-Kreitman, Tajima's D, Fu and Li's D and F, Fay and Wu's H) statistics in sympatric and allopatric populations of two distinct forms of C. intestinalis (Types A and B) between which there are strong post-zygotic barriers.     

Divergent landscape effects on population connectivity in two co-occurring amphibian species

The physical and environmental attributes of landscapes often shape patterns of population connectivity by influencing dispersal and gene flow. Landscape effects on movement are typically evaluated for single species. However, inferences from multiple species are required for multi‐species management strategies increasingly being applied in conservation. In this study, I compared the spatial genetic patterns of two amphibian species across the northeastern United States and estimated the influence of specific landscape features on the observed genetic structure. The spotted salamander (Ambystoma maculatum) and wood frog (Rana sylvatica) share many ecological attributes related to habitat use, phenology and site fidelity. However, I hypothesized that important differences in their movement patterns and life history would create distinct genetic patterns for each species. Using 14 microsatellite loci, I tested for differences in the level of genetic differentiation between the two species across 22 breeding ponds. The effects of eight landscape features were also estimated by evaluating 32 landscape resistance models. Spotted salamanders exhibited significantly higher genetic differentiation than wood frogs. Different landscape features were also identified as potential drivers of the genetic patterns in each species, with little overlap in model support between species. Collectively, these results provide strong evidence that these two amphibian species interact with the landscape in measurably different ways. The distinct genetic patterns observed are consistent with key differences in movement ability and life history between A. maculatum and R. sylvatica. These results highlight the importance of considering more than one species when assessing the impacts of the landscape matrix on population connectivity, even for ecologically similar species within the same habitats.     

Habitat selection of three cryptic Plecotus bat species in the European Alps reveals contrasting implications for conservation

Assessing the ecological requirements of species coexisting within a community is an essential requisite for developing sound conservation action. A particularly interesting question is what mechanisms govern the stable coexistence of cryptic species within a community, i.e. species that are almost impossible to distinguish. Resource partitioning theory predicts that cryptic species, like other sympatric taxa, will occupy distinct ecological niches. This prediction is widely inferred from eco-morphological studies. A new cryptic long-eared bat species, Plecotus macrobullaris, has been recently discovered in the complex of two other species present in the European Alps, with even evidence for a few mixed colonies. This discovery poses challenges to bat ecologists concerned with planning conservation measures beyond roost protection. We therefore tested whether foraging habitat segregation occurred among the three cryptic Plecotus bat species in Switzerland by radiotracking 24 breeding female bats (8 of each species). We compared habitat features at locations visited by a bat versus random locations within individual home ranges, applying mixed effects logistic regression. Distinct, species-specific habitat preferences were revealed. P. auritus foraged mostly within traditional orchards in roost vicinity, with a marked preference for habitat heterogeneity. P. austriacus foraged up to 4.7 km from the roost, selecting mostly fruit tree plantations, hedges and tree lines. P. macrobullaris preferred patchy deciduous and mixed forests with high vertical heterogeneity in a grassland dominated-matrix. These species-specific habitat preferences should inform future conservation programmes. They highlight the possible need of distinct conservation measures for species that look very much alike.     

Morphology, echolocation and foraging behaviour in two sympatric sibling species of bat (Tylonycteris pachypus and Tylonycteris robustula) (Chiroptera: Vespertilionidae)

We studied the wing morphology, echolocation calls, foraging behaviour and flight speed of Tylonycteris pachypus and Tylonycteris robustula in Longzhou County, South China during the summer (June–August) of 2005. The wingspan, wing loading and aspect ratio of the two species were relatively low, and those of T. pachypus were lower compared with T. robustula . The echolocation calls of T. pachypus and T. robustula consist of a broadband frequency modulated (FM) sweep followed by a short narrowband FM sweep. The dominant frequency of calls of T. pachypus was 65.1 kHz, whereas that of T. robustula was 57.7 kHz. The call frequencies (including highest frequency of the call, lowest frequency of the call and frequency of the call that contained most energy) of T. pachypus were higher than those of T. robustula , and the pulse duration of the former was longer than that of the latter. The inter-pulse interval and bandwidth of the calls were not significantly different between the two species. Tylonycteris pachypus foraged in more complex environments than T. robustula , although the two species were both netted in edge habitats (around trees or houses), along pathways and in the tops of trees. Tylonycteris pachypus flew slower (straight level flight speed, 4.3 m s⁻¹) than T. robustula (straight level flight speed, 4.8 m s⁻¹). We discuss the relationship between wing morphology, echolocation calls, foraging behaviour and flight speed, and demonstrate resource partitioning between these two species in terms of morphological and behavioural factors.     

Contrasting genetic structure in two co-distributed species of old world fruit bat

The fulvous fruit bat (Rousettus leschenaulti) and the greater short-nosed fruit bat (Cynopterus sphinx) are two abundant and widely co-distributed Old World fruit bats in Southeast and East Asia. The former species forms large colonies in caves while the latter roots in small groups in trees. To test whether these differences in social organization and roosting ecology are associated with contrasting patterns of gene flow, we used mtDNA and nuclear loci to characterize population genetic subdivision and phylogeographic histories in both species sampled from China, Vietnam and India. Our analyses from R. leschenaulti using both types of marker revealed little evidence of genetic structure across the study region. On the other hand, C. sphinx showed significant genetic mtDNA differentiation between the samples from India compared with China and Vietnam, as well as greater structuring of microsatellite genotypes within China. Demographic analyses indicated signatures of past rapid population expansion in both taxa, with more recent demographic growth in C. sphinx. Therefore, the relative genetic homogeneity in R. leschenaulti is unlikely to reflect past events. Instead we suggest that the absence of substructure in R. leschenaulti is a consequence of higher levels of gene flow among colonies, and that greater vagility in this species is an adaptation associated with cave roosting.     

Differences in oviposition behaviour of two sympatric sibling species of the genus Ostrinia

Changes in host preferences are thought to be a major source of genetic divergence between phytophagous insect taxa. In western Europe, two sympatric taxa, O. nubilalis (the European corn borer) and O. scapulalis, feed mainly on maize and hop or mugwort, respectively. These two species may have diverged without geographic isolation after a host shift of ancestral populations onto maize or another cultivated species (e.g. sorghum). A previous study using inbred laboratory strains revealed that the two species differ in their oviposition choices in maize-mugwort tests. We sampled four natural populations in France (two of each taxon) and tested their oviposition behaviour toward four of their main host plant species: maize, sorghum, mugwort and hop. O. nubilalis females showed a very high preference for laying their eggmasses on maize, whereas O. scapulalis females displayed a more balanced range of preferences. O. nubilalis females were attracted slightly to sorghum, suggesting that this plant is an accidental, rather than a regular and ancestral host plant of O. nubilalis. One important result arising from this study is the significant proportion of eggs laid by both Ostrinia species on hop. This may explain why some stands of hop are sometimes not only infested by O. scapulalis but also by O. nubilalis larvae, a situation preventing assortative mating based on microallopatry. Hence, further studies must be conducted to see whether the host preference in the genus Ostrinia might be linked to assortative mating by a mechanism that is not mediated by the host plant.     

DNA barcode discovers two cryptic species and two geographical radiations in the invasive drosophilid Zaprionus indianus

Comparing introduced to ancestral populations within a phylogeographical context is crucial in any study aiming to understand the ecological genetics of an invasive species. Zaprionus indianus is a cosmopolitan drosophilid that has recently succeeded to expand its geographical range upon three continents (Africa, Asia and the Americas). We studied the distribution of mitochondrial DNA (mtDNA) haplotypes for two genes (CO‐I and CO‐II) among 23 geographical populations. mtDNA revealed the presence of two well‐supported phylogenetic lineages (phylads), with bootstrap value of 100%. Phylad I included three African populations, reinforcing the African‐origin hypothesis of the species. Within phylad II, a distinct phylogeographical pattern was discovered: Atlantic populations (from the Americas and Madeira) were closer to the ancestral African populations than to Eastern ones (from Madagascar, Middle East and India). This means that during its passage from endemism to cosmopolitanism, Z. indianus exhibited two independent radiations, the older (the Eastern) to the East, and the younger (the Atlantic) to the West. Discriminant function analysis using 13 morphometrical characters was also able to discriminate between the two molecular phylads (93.34 ± 1.67%), although detailed morphological analysis of male genitalia using scanning electron microscopy showed no significant differences. Finally, crossing experiments revealed the presence of reproductive barrier between populations from the two phylads, and further between populations within phylad I. Hence, a bona species status was assigned to two new, cryptic species: Zaprionus africanus and Zaprionus gabonicus, and both were encompassed along with Z. indianus and Zaprionus megalorchis into the indianus complex. The ecology of these two species reveals that they are forest dwellers, which explains their restricted endemic distribution, in contrast to their relative cosmopolitan Z. indianus, known to be a human‐commensal. Our results reconfirm the great utility of mtDNA at both inter‐ and intraspecific analyses within the frame of an integrated taxonomical project.     

Antennal sensilla of two female anopheline sibling species with differing host ranges

Background

Malaria control strategies emphasize the need for prompt and effective treatment of malaria episodes. To increase treatment efficacy, Tanzania changed its first-line treatment from chloroquine to sulphadoxine-pyrimethamine (SP) in 2001. The effect of this policy change on the availability of antimalarials was studied in rural south-eastern Tanzania.

Methods

In 2001 and 2004, the study area was searched for commercial outlets selling drugs and their stocks were recorded. Household information was obtained from the local Demographic Surveillance System.

Results

From 2001 to 2004, the number of general shops stocking drugs increased by 15% and the number of drug stores nearly doubled. However, the proportion of general shops stocking antimalarials dropped markedly, resulting in an almost 50% decrease of antimalarial selling outlets. This led to more households being located farther from a treatment source. In 2004, five out of 25 studied villages with a total population of 13,506 (18%) had neither a health facility, nor a shop as source of malaria treatment.

Conclusion

While the change to SP resulted in a higher treatment efficacy, it also led to a decreased antimalarial availability in the study area. Although there was no apparent impact on overall antimalarial use, the decline in access may have disproportionately affected the poorest and most remote groups. In view of the imminent policy change to artemisinin-based combination therapy these issues need to be addressed urgently if the benefits of this new class of antimalarials are to be extended to the whole population.     

Resolving the trophic relations of cryptic species: an example using stable isotope analysis of dolphin teeth

Understanding the foraging ecology and diet of animals can play a crucial role in conservation of a species. This is particularly true where species are cryptic and coexist in environments where observing feeding behaviour directly is difficult. Here we present the first information on the foraging ecology of a recently identified species of dolphin (Southern Australian bottlenose dolphin (SABD)) and comparisons to the common bottlenose dolphin (CBD) in Victoria, Australia, using stable isotope analysis of teeth. Stable isotope signatures differed significantly between SABD and CBD for both δ(13)C (-14.4‰ vs. -15.5‰ respectively) and δ(15)N (15.9‰ vs. 15.0‰ respectively), suggesting that the two species forage in different areas and consume different prey. This finding supports genetic and morphological data indicating that SABD are distinct from CBD. In Victoria, the SABD is divided into two distinct populations, one in the large drowned river system of Port Phillip Bay and the other in a series of coastal lakes and lagoons called the Gippsland Lakes. Within the SABD species, population differences were apparent. The Port Phillip Bay population displayed a significantly higher δ(15)N than the Gippsland Lakes population (17.0‰ vs. 15.5‰), suggesting that the Port Phillip Bay population may feed at a higher trophic level--a result which is supported by analysis of local food chains. Important future work is required to further understand the foraging ecology and diet of this newly described, endemic, and potentially endangered species of dolphin.     

Abrupt evolutionary change in the Balbiani ring gene family in two sibling species ofChironomus

Summary We have investigated interspecific divergence in a eucaryotic gene family, the Balbiani ring genes of the dipteran genusChironomus. In general, our data show thatC. pallidivittatus andC. tentans possess virtually identical Balbiani ring gene sequences, whereasC. thummi represents a more distantly related member of the genus. These results are consistent with phylogenetic relationships for the three species based on polytene chromosome banding patterns. However, one Balbiani ring gene sequence displays an evolutionarily anomalous behavior. A 16-kilobase-pair Balbiani ring gene 1 sequence inC. pallidivittatus that we show to be transcribed is absent in the sibling speciesC. tentans. We propose that this sequence was deleted inC. tentans after divergence of the species. Considering the importance of Balbiani ring genes for feeding and protection of theChironomus larvae, we suggest that the pronounced interspecific genetic difference contributes to a difference in ecological niche between the two sympatrically distributed species.     

Micro-spatial distribution of two sibling periwinkle species across the intertidal indicates hybrdization

Populations of periwinkles Littorina saxatilis (Olivi 1792) and L. arcana Hannaford Ellis, 1978 are well suited for microevolutionary studies, being at the same time closely related and intraspecifically diverse. The divergence between these two sibling species, sympatric over large parts of their distribution areas, is small, the only morphological difference being the pallial gland complex structure in females. Molecular identification is possible with the use of a RAPD nuclear marker (cloned A2.8 DNA fragment) typical for L. arcana. However, in some individuals from sympatric populations molecular and morphological criteria suggest conflicting species affiliation, which may be explained either by hybridization or by shared ancestral polymorphism. We tested the hybridization hypotheses examining the micro-spatial distribution of these two species across the intertidal zone in two distant sites at the Barents Sea. We found that (a) the frequency of putative hybrids in sympatric populations was proportional to the frequency of L. arcana; (b) L. saxatilis bearing A2.8 DNA fragment were almost absent in the lower part of the intertidal zone, where L. arcana was absent too; (c) there was a close positive correlation between the distribution of potential parent molluscs and putative hybrids. Moreover, logistic regression models showed a good agreement between the distribution of putative hybrid frequencies and that of parental species frequencies. All our observations taken together support the hypothesis of hybridization between L. saxatilis and L. arcana. Elucidating the mechanisms that support the species status of these sympatric populations is necessary.     

Algal species composition and phosphorus recycling at contrasting grazing pressure: an experimental study in sub-Antarctic lakes with two trophic levels

1. To test the response of algal communities to altered grazer abundance in lakes lacking efficient predators on herbivores, we performed field and experimental studies in two sub-Antarctic lakes (South Georgia).
2. The number of algal species in these high latitude lakes is low, and all dominant species have grazer-resistant adaptations, including spines in three dimensions ( Staurastrum sp.), large size ( Tribonema sp.), a mucus sheet allowing viable passage through the gut ( Chlamydocapsa sp., Elakatothrix sp.) or ability to recruit individuals from the sediment surface ( Mallomonas sp.).
3. Algal community composition was only slightly changed by experimentally altered grazer abundance, indicating that it was already adapted for a high grazing pressure. Hence, the diets of herbivores were restricted to vulnerable food organisms such as Mallomonas sp. and heterotrophic flagellates in the water column, and to benthic food sources.
4. At high grazer abundance, the concentration of available phosphorus (PO₄-P) in the water was lower than at low grazer abundances, due to inefficient nutrient regeneration by the copepod herbivores. Hence, in lakes where copepods are dominant grazers, algae suffer both directly from grazing and indirectly from reduced nutrient availability.     

Algal species composition and phosphorus recycling at contrasting grazing pressure: an experimental study in sub-Antarctic lakes with two trophic levels

1. To test the response of algal communities to altered grazer abundance in lakes lacking efficient predators on herbivores, we performed field and experimental studies in two sub-Antarctic lakes (South Georgia).
2. The number of algal species in these high latitude lakes is low, and all dominant species have grazer-resistant adaptations, including spines in three dimensions ( Staurastrum sp.), large size ( Tribonema sp.), a mucus sheet allowing viable passage through the gut ( Chlamydocapsa sp., Elakatothrix sp.) or ability to recruit individuals from the sediment surface ( Mallomonas sp.).
3. Algal community composition was only slightly changed by experimentally altered grazer abundance, indicating that it was already adapted for a high grazing pressure. Hence, the diets of herbivores were restricted to vulnerable food organisms such as Mallomonas sp. and heterotrophic flagellates in the water column, and to benthic food sources.
4. At high grazer abundance, the concentration of available phosphorus (PO₄-P) in the water was lower than at low grazer abundances, due to inefficient nutrient regeneration by the copepod herbivores. Hence, in lakes where copepods are dominant grazers, algae suffer both directly from grazing and indirectly from reduced nutrient availability.