Size and structure of populations of Oedura reticulata (Reptilia: Gekkonidae) in woodland remnants: Implications for the future regional distribution of a currently common species

Abstract The gecko Oedura reticulata is restricted in distribution to the southwest of Western Australia. Within this region O. reticulata occurs mainly in smooth-barked eucalypt woodland habitat, much of which has become fragmented by clearing. In this study, demographic characteristics of nine populations of O. reticulata that currently persist in eucalypt woodland remnants are assessed and compared with those of populations in three nature reserves. The remnants cover a range of sizes but are similar in age, tree species composition and vegetation structure. Population sizes vary considerably among remnants and are poorly correlated with remnant size or the number of smooth-barked eucalypts. Population size does not appear to be limited by habitat availability in most remnants. The number of adults of breeding age is small in most populations suggesting that they may be susceptible to stochastic extinction pressures. The poor dispersal ability of this species between remnants means that the possibility of recolonization of a remnant following an extinction event is unlikely. As a result, the occupancy rate of O. reticulata in remnant woodland is likely to decline.     

Tetranucleotide microsatellites in the gecko Oedura reticulata isolated from an enriched library

Ten tetranucleotide microsatellite loci were isolated from an enriched library for the gecko Oedura reticulata. The species is endemic to the southwest of Western Australia, known to be a habitat specialist, and exposed to severe habitat fragmentation in the Western Australian wheatbelt. These highly polymorphic markers (two to 25 alleles) will facilitate the population genetic analyses of this species. In particular, they will enable estimates of gene flow between remnant populations — a critical element in assessing extinction dynamics in fragmented populations.     

Mitochondrial DNA variation among populations of Oedura reticulata (Gekkonidae) in remnant vegetation: implications for metapopulation structure and population decline

Restriction fragment length polymorphism (RFLP) analysis of mitochondrial DNA was used to examine the regional population structure of a species of gecko (Oedura reticulata) in vegetation remnants within the Western Australian wheatbelt. The species exhibited considerable polymorphism within and between populations with 22 haplotypes recognized among 12 populations. Phylogenetic analysis of haplotypes and clustering of nucleotide divergence among populations demonstrated little regional structure within the species with several haplotypes present in all three regions surveyed. This contrasted markedly with variation in haplotype frequency among populations which showed a high degree of independence between populations indicating that current levels of maternal gene flow are low and that the populations are too small to prevent genetic drift. This conclusion is supported by generally lower numbers of haplotypes in remnant populations than in nearby nature reserves. These findings, combined with demographic data from a previous study, suggest that post-fragmentation populations of O. reticulata are unable to form a metapopulation structure in the habitat that remains and that stochastic extinction forces alone will be sufficient to severely reduce the regional distribution of this species. This study demonstrates that mtDNA is a useful tool for detecting contemporary population phenomena and can provide qualitative information of practical importance to wildlife managers.     

The tales of two geckos: does dispersal prevent extinction in recently fragmented populations?

Although habitat loss and fragmentation threaten species throughout the world and are a major threat to biodiversity, it is apparent that some species are at greater risk of extinction in fragmented landscapes than others. Identification of these species and the characteristics that make them sensitive to habitat fragmentation has important implications for conservation management. Here, we present a comparative study of the population genetic structure of two arboreal gecko species (Oedura reticulata and Gehyra variegata) in fragmented and continuous woodlands. The species differ in their level of persistence in remnant vegetation patches (the former exhibiting a higher extinction rate than the latter). Previous demographic and modelling studies of these two species have suggested that their difference in persistence levels may be due, in part, to differences in dispersal abilities with G. variegata expected to have higher dispersal rates than O. reticulata. We tested this hypothesis and genotyped a total of 345 O. reticulata from 12 sites and 353 G. variegata from 13 sites at nine microsatellite loci. We showed that O. reticulata exhibits elevated levels of structure (FST=0.102 vs. 0.044), lower levels of genetic diversity (HE=0.79 vs. 0.88), and fewer misassignments (20% vs. 30%) than similarly fragmented populations of G. variegata, while all these parameters were fairly similar for the two species in the continuous forest populations (FST=0.003 vs. 0.004, HE=0.89 vs. 0.89, misassignments: 58% vs. 53%, respectively). For both species, genetic structure was higher and genetic diversity was lower among fragmented populations than among those in the nature reserves. In addition, assignment tests and spatial autocorrelation revealed that small distances of about 500 m through fragmented landscapes are a barrier to O. reticulata but not for G. variegata. These data support our hypothesis that G. variegata disperse more readily and more frequently than O. reticulata and that dispersal and habitat specialization are critical factors in the persistence of species in habitat remnants.     

Habitat connectivity, more than species’ biology, influences genetic differentiation in a habitat specialist, the short-eared rock-wallaby (Petrogale brachyotis)

It is difficult to assess the relative influence of anthropogenic processes (e.g., habitat fragmentation) versus species’ biology on the level of genetic differentiation among populations when species are restricted in their distribution to fragmented habitats. This issue is particularly problematic for Australian rock-wallabies (Petrogale sp.), where most previous studies have examined threatened species in anthropogenically fragmented habitats. The short-eared rock-wallaby (Petrogale brachyotis) provides an opportunity to assess natural population structure and gene flow in relatively continuous habitat across north-western Australia. This region has reported widespread declines in small-to-medium sized mammals, making data regarding the influence of habitat connectivity on genetic diversity important for broad-scale management. Using non-invasive and standard methods, 12 microsatellite loci and mitochondrial DNA were compared to examine patterns of population structure and dispersal among populations of P. brachyotis in the Kimberley, Western Australia. Low genetic differentiation was detected between populations separated by up to 67?km. The inferred genetic connectivity of these populations suggests that in suitable habitat P. brachyotis can potentially disperse far greater distances than previously reported for rock-wallabies in more fragmented habitat. Like other Petrogale species male-biased dispersal was detected. These findings suggest that a complete understanding of population biology may not be achieved solely by the study of fragmented populations in disturbed environments and that management strategies may need to draw on studies of populations (or related species) in undisturbed areas of contiguous habitat.     

Niche divergence promotes rapid diversification of East African sky island white‐eyes (Aves: Zosteropidae)

The Eastern Afromontane biodiversity hotspot composed of highly fragmented forested highlands (sky islands) harbours exceptional diversity and endemicity, particularly within birds. To explain their elevated diversity within this region, models founded on niche conservatism have been offered, although detailed phylogeographic studies are limited to a few avian lineages. Here, we focus on the recent songbird genus Zosterops, represented by montane and lowland members, to test the roles of niche conservatism versus niche divergence in the diversification and colonization of East Africa's sky islands. The species‐rich white‐eyes are a typically homogeneous family with an exceptional colonizing ability, but in contrast to their diversity on oceanic islands, continental diversity is considered depauperate and has been largely neglected. Molecular phylogenetic analysis of ~140 taxa reveals extensive polyphyly among different montane populations of Z. poliogastrus. These larger endemic birds are shown to be more closely related to taxa with divergent habitat types, altitudinal distributions and dispersal abilities than they are to populations of restricted endemics that occur in neighbouring montane forest fragments. This repeated transition between lowland and highland habitats over time demonstrate that diversification of the focal group is explained by niche divergence. Our results also highlight an underestimation of diversity compared to morphological studies that has implications for their taxonomy and conservation. Molecular dating suggests that the spatially extensive African radiation arose exceptionally rapidly (1–2.5 Ma) during the fluctuating Plio‐Pleistocene climate, which may have provided the primary driver for lineage diversification.     

Does isolation affect phenotypic variability and fluctuating asymmetry in the endangered Red Apollo?

Isolated populations represent one of the main focuses in conservation biology. Long-term isolation often causes losses of genetic diversity and as a consequence might reduce individual fitness. Morphometric characters can be used as suitable markers to analyse ecological stress and individual fitness of local populations. Asymmetry in bilateral symmetry is used as a measure for developmental instability of populations and is often negatively correlated with population size and low genetic diversity. As a study system, we selected the endangered butterfly Parnassius apollo, which occurs in small and isolated remnant populations in Central Europe, but also in fairly large metapopulations in the Alps. We analysed wing morphometrics (shape and size characters) of 812 individuals representing (1) already extinct, (2) highly isolated and (3) still interconnected populations. Seventeen landmarks on veins were used to analyse morphological variances in the wing shape. Our data show significant deviations between landmarks on the left and right wing side within individuals and strong morphological variance among individuals. The highest morphological variability could be found for individuals in the Alps, however, the level of asymmetry was very similar for all populations analysed. The higher morphological variability found in the Alps can be interpreted as a consequence of the higher level of the genetic diversity detectable for this region. Analysis on morphological variance of P. apollo individuals of the Mosel valley using time series ranging from 1895 until today showed no significant rise in asymmetry and no decline of morphological variability over time, although, anthropogenic habitat destruction has caused severe bottlenecks in this population.     

The comparative biogeography of Philippine geckos challenges predictions from a paradigm of climate‐driven vicariant diversification across an island archipelago

A primary goal of biogeography is to understand how large‐scale environmental processes, like climate change, affect diversification. One often‐invoked but seldom tested process is the “species‐pump” model, in which repeated bouts of cospeciation are driven by oscillating climate‐induced habitat connectivity cycles. For example, over the past three million years, the landscape of the Philippine Islands has repeatedly coalesced and fragmented due to sea‐level changes associated with glacial cycles. This repeated climate‐driven vicariance has been proposed as a model of speciation across evolutionary lineages codistributed throughout the islands. This model predicts speciation times that are temporally clustered around the times when interglacial rises in sea level fragmented the islands. To test this prediction, we collected comparative genomic data from 16 pairs of insular gecko populations. We analyze these data in a full‐likelihood, Bayesian model‐choice framework to test for shared divergence times among the pairs. Our results provide support against the species‐pump model prediction in favor of an alternative interpretation, namely that each pair of gecko populations diverged independently. These results suggest the repeated bouts of climate‐driven landscape fragmentation have not been an important mechanism of speciation for gekkonid lizards across the Philippine Archipelago.     

Genetic analysis reveals the costs of peri-urban development for the endangered grassland earless dragon

Australia’s natural temperate grasslands have diminished to 0.5 % of their former area since European settlement and, as a consequence, are highly fragmented and modified. Many vertebrate species that live in temperate grasslands are habitat specialists and therefore are at risk of decline through habitat loss and fragmentation. The grassland earless dragon (Tympanocryptis pinguicolla) is one such species. Once widespread, T. pinguicolla is now restricted to two general locations; the first is near Canberra in the Australian Capital Territory (including some adjacent land near Queanbeyan), and the second is the Monaro Tablelands in New South Wales. Here, we use microsatellite DNA data collected from the largest remaining populations near Canberra to examine genetic structure in this species in the context of the rapidly expanding urban landscape in this region. Our study revealed that, despite separation by only relatively small distances (largest distance ~13 km), the T. pinguicolla populations are highly genetically structured with little admixture. Our analyses also revealed that the population with the largest census size, but which has recently crashed in population size, exhibited little detectable gene flow to other populations and is essentially isolated. Our data indicate that significant barriers to dispersal exist among the remaining T. pinguicolla populations and that management of this species cannot rely on natural dispersal to bolster declining populations. Many different agencies and landholders are responsible for the protection of these remnant populations and a co-ordinated effort is required to provide reasonable confidence that the species will persist.     

Adaptive radiation in Lesser Antillean lizards: molecular phylogenetics and species recognition in the Lesser Antillean dwarf gecko complex, Sphaerodactylus fantasticus

The time associated with speciation varies dramatically among lower vertebrates. The nature and timing of divergence is investigated in the fantastic dwarf gecko Sphaerodactylus fantasticus complex, a nominal species that occurs on the central Lesser Antillean island of Guadeloupe and adjacent islands and islets. This is compared to the divergence in the sympatric anole clade from the Anolis bimaculatus group. A molecular phylogenetic analysis of numerous gecko populations from across these islands, based on three mitochondrial DNA genes, reveals several monophyletic groups occupying distinct geographical areas, these being Les Saintes, western Basse Terre plus Dominica, eastern Basse Terre, Grand Terre, and the northern and eastern islands (Montserrat, Marie Galante, Petite Terre, Desirade). Although part of the same nominal species, the molecular divergence within this species complex is extraordinarily high (27% patristic distance between the most divergent lineages) and is compatible with this group occupying the region long before the origin of the younger island arc. Tests show that several quantitative morphological traits are correlated with the phylogeny, but in general the lineages are not uniquely defined by these traits. The dwarf geckos show notably less nominal species-level adaptive radiation than that found in the sympatric southern clade of Anolis bimculatus , although both appear to have occupied the region for a broadly similar period of time. Nevertheless, the dwarf gecko populations on Les Saintes islets are the most morphologically distinct and are recognized as a full species ( Sphaerodactylus phyzacinus ), as are anoles on Les Saintes ( Anolis terraealtae ).     

Multiple speciation events in an arthropod with divergent evolution in sexual morphology

Sexual selection can facilitate divergent evolution of traits related to mating and consequently promote speciation. Theoretically, independent operation of sexual selection in different populations can lead to divergence of sexual traits among populations and result in allopatric speciation. Here, we show that divergent evolution in sexual morphology affecting mating compatibility (body size and genital morphologies) and speciation have occurred in a lineage of millipedes, the Parafontaria tonominea species complex. In this millipede group, male and female body and genital sizes exhibit marked, correlated divergence among populations, and the diverged morphologies result in mechanical reproductive isolation between sympatric species. The morphological divergence occurred among populations independently and without any correlation with climatic variables, although matching between sexes has been maintained, suggesting that morphological divergence was not a by-product of climatic adaptation. The diverged populations underwent restricted dispersal and secondary contact without hybridization. The extent of morphological difference between sympatric species is variable, as is diversity among allopatric populations; consequently, the species complex appears to contain many species. This millipede case suggests that sexual selection does contribute to species richness via morphological diversification when a lineage of organisms consists of highly divided populations owing to limited dispersal.     

Genetic structure of a native cyprinid in a reservoir‐altered stream network

1. Reservoirs modify riverine ecosystems worldwide, and often with deleterious impacts on native biota. The immediate effects of reservoirs on native fish species below dams and in impounded reaches have received considerable attention, but it is unclear how reservoirs may affect fish species at larger spatial and temporal scales. Documented declines of stream fish populations in direct tributaries of reservoirs suggest reservoir pools may reduce gene flow among historically connected populations. 2. Because of increased predator densities in reservoirs and the extent of habitat alteration in impounded reaches, I predicted reservoir habitats would reduce gene flow among small‐bodied fish populations separated by reservoir habitat. I used microsatellite markers to assess the spatial genetic structure of populations of the red shiner (Cyprinella lutrensis), in a reservoir‐fragmented stream network (Lake Texoma, U.S.A.). I also tested the prediction that populations in two direct tributaries that have experienced population declines would have low genetic diversity. Individuals were collected from six sites upstream of the reservoir, three sites in the reservoir and three sites in direct tributaries of the reservoir during 2008 and 2009. 3. Results indicate that most populations were isolated by distance with little divergence among populations. In one direct tributary population, however, there was substantial genetic divergence, and genetic diversity was significantly lower than in other populations. Gene flow also seemed to be lower in reservoir habitats than in intact stream habitats, suggesting reservoir habitats may be reducing gene flow among the reservoir‐separated populations. These results indicate that reservoirs may reduce gene flow among reservoir‐fragmented stream fish populations, altering the evolutionary trajectories of fragmented populations.     

A cryptic and critically endangered species revealed by mitochondrial DNA analyses: the Western Ground Parrot

We examined cytochrome b sequence data to resolve the intraspecific taxonomy of ground parrots Pezoporus wallicus. The species occurs in fragmented coastal heaths in south-eastern and south-western Australia. Net nucleotide divergences among all eastern populations were very low (0.0–0.6%) and genetic diversity unstructured, suggesting relatively recent common ancestry. Gene flow among them was probably maintained via land bridges and the persistence of suitable habitat during the Pleistocene. In contrast, net nucleotide divergence was high (4.4–5.1%) between western and eastern populations, suggesting more ancient divergence about 2 million years ago. The magnitude of divergence between eastern and western lineages is similar to a wide range of avian congeners. Our data support the need to reconsider the intraspecific taxonomy of ground parrots, and we cautiously suggest the recognition of Western Ground Parrots as a species, P. flaviventris, for conservation prioritization, planning and management purposes. Given their recent precipitous decline to approximately 110 individuals, most of which occur at one location, this makes Western Ground Parrots one of the world’s most threatened bird species.     

Contrasting genetic responses to population fragmentation in a coevolving fig and fig wasp across a mainland–island archipelago

Interacting species of pollinator–host systems, especially the obligate ones, are sensitive to habitat fragmentation, due to the nature of mutual dependence. Comparative studies of genetic structure can provide insights into how habitat fragmentation contributes to patterns of genetic divergence among populations of the interacting species. In this study, we used microsatellites to analyse genetic variation in Chinese populations of a typical mutualistic system – Ficus pumila and its obligate pollinator Wiebesia sp. 1 – in a naturally fragmented landscape. The plants and wasps showed discordant patterns of genetic variation and geographical divergence. There was no significant positive relationship in genetic diversity between the two species. Significant isolation‐by‐distance (IBD) patterns occurred across the populations of F. pumila and Wiebesia sp. 1 as whole, and IBD also occurred among island populations of the wasps, but not the plants. However, there was no significant positive relationship in genetic differentiation between them. The pollinator populations had significantly lower genetic variation in small habitat patches than in larger patches, and three island pollinator populations showed evidence of a recent bottleneck event. No effects of patch size or genetic bottlenecks were evident in the plant populations. Collectively, the results indicate that, in more fragmented habitats, the pollinators, but not the plants, have experienced reduced genetic variation. The contrasting patterns have multiple potential causes, including differences in longevity and hence number of generations experiencing fragmentation; different dispersal patterns, with the host's genes dispersed as seeds as well as a result of pollen dispersal via the pollinator; asymmetrical responses to fluctuations in partner populations; and co‐existence of a rare second pollinating wasp on some islands. These results indicate that strongly interdependent species may respond in markedly different ways to habitat fragmentation.     

Landscape configuration determines gene flow and phenotype in a flightless forest-edge ground-dwelling bush-cricket, Pholidoptera griseoaptera

Spatial configuration of habitats influences genetic structure and population fitness whereas it affects mainly species with limited dispersal ability. To reveal how habitat fragmentation determines dispersal and dispersal-related morphology in a ground-dispersing insect species we used a bush-cricket (Pholidoptera griseoaptera) which is associated with forest-edge habitat. We analysed spatial genetic patterns together with variability of the phenotype in two forested landscapes with different levels of fragmentation. While spatial configuration of forest habitats did not negatively affect genetic characteristics related to the fitness of sampled populations, genetic differentiation was found higher among populations from an extensive forest. Compared to an agricultural matrix between forest patches, the matrix of extensive forest had lower permeability and posed barriers for the dispersal of this species. Landscape configuration significantly affected also morphological traits that are supposed to account for species dispersal potential; individuals from fragmented forest patches had longer hind femurs and a higher femur to pronotum ratio. This result suggests that selection pressure act differently on populations from both landscape types since dispersal-related morphology was related to the level of habitat fragmentation. Thus observed patterns may be explained as plastic according to the level of landscape configuration; while anthropogenic fragmentation of habitats for this species can lead to homogenization of spatial genetic structure.     

Water availability strongly impacts population genetic patterns of an imperiled Great Plains endemic fish

Genetic, demographic, and environmental processes affect natural populations synergistically, and understanding their interplay is crucial for the conservation of biodiversity. Stream fishes in metapopulations are particularly sensitive to habitat fragmentation because persistence depends on dispersal and colonization of new habitat but dispersal is constrained to stream networks. Great Plains streams are increasingly fragmented by water diversion and climate change, threatening connectivity of fish populations in this ecosystem. We used seven microsatellite loci to describe population and landscape genetic patterns across 614 individuals from 12 remaining populations of Arkansas darter (Etheostoma cragini) in Colorado, a candidate species for listing under the U.S. Endangered Species Act. We found small effective population sizes, low levels of genetic diversity within populations, and high levels of genetic structure, especially among basins. Both at- and between-site landscape features were associated with genetic diversity and connectivity, respectively. Available stream habitat and amount of continuous wetted area were positively associated with genetic diversity within a site, while stream distance and intermittency were the best predictors of genetic divergence among sites. We found little genetic contribution from historic supplementation efforts, and we provide a set of management recommendations for this species that incorporate a conservation genetics perspective.     

Assessing non-metric skeleton characters as a morphological tool

The appearance of non-metric skeletal characters in vertebrates results mainly from basic genetic control, as proved and documented for house mice and humans. Although the heritability of non-metric traits, mainly the presence of foramina and similar structures for blood vessels and nerves or dental occlusal variants, have been evaluated as rather low, the simultaneous consideration of several traits allows estimation of epigenetic variation in time and space as a result of genetic relationship. Thus, the main use of non-metric characters has been aimed at assessing epigenetic variability and divergence among populations. Applications extend from the problem of genetic isolation of populations, the lack of reproductive contact, detection of genetic drift, systematic studies to clarify species taxonomy, to phylogenetic interpretation.

Additionally, non-directional deviations from bilateral symmetry in non-metric characters, e.g. fluctuating asymmetry, could be caused by current environmental conditions in general. Fluctuating asymmetry is regarded as a measure of developmental instability to indicate the presence of genomic changes or the influence of contamination and/or habitat deterioration, and is also used as a further population parameter with integrated information. However, standpoints on the use of fluctuating asymmetry are quite inconsistent, fluctuating themselves between considering it a powerful biomonitoring tool to being merely a curious scientific toy.     

Conservation genetics and breeding system of Penstemon debilis (Plantaginaceae), a rare beardtongue endemic to oil shale talus in western Colorado,USA

Rare species of plants are especially vulnerable to extinction when populations are few, have small numbers of individuals, and are fragmented. Such conditions lead to a reduction in gene flow and genetic diversity, and encourage inbreeding depression. We conducted a study of the reproductive biology and population genetics of Penstemon debilis (Plantaginaceae), a Federally Threatened species endemic to a small region of oil shale extraction in western Colorado, USA. Most of the habitat area is privately owned and undergoing natural gas extraction activities. Penstemon debilis reproduces both vegetatively and as an outcrosser that requires a pollen vector. Moderate levels of inbreeding, but no inbreeding depression, were found within populations of P. debilis. Genetic divergence among the extant populations surveyed was moderate (F_ST values = 0.069–0.231; Nm = 0.831–3.385) with levels of genetic diversity within populations relatively low compared to congeners with similar modes of pollination and reproductive biology. STRUCTURE analysis revealed three population clusters with some admixture among all extant populations. Genetic diversity within and among P. debilis populations is similar to genetic diversity found for other rare and endemic outcrossing plant species. Our results are consistent with a pattern of recent population fragmentation or low levels of pollen‐mediated gene flow among populations in close proximity to one another. Conservation of P. debilis will require cooperative management strategies between private landowners, government agencies, and concerned NGOs to preserve habitat for this rare species.     

Genetic Differentiation and Demographic History of the Northern Rufous Mouse Lemur (<Emphasis Type="Italic">Microcebus tavaratra</Emphasis>) Across a Fragmented Landscape in Northern Madagascar

Phylogeographic barriers, together with habitat loss and fragmentation, contribute to the evolution of a species’ genetic diversity by limiting gene flow and increasing genetic differentiation among populations. Changes in connectivity can thus affect the genetic diversity of populations, which may influence the evolutionary potential of species and the survival of populations in the long term. We studied the genetic diversity of the little known Northern rufous mouse lemur (Microcebus tavaratra), endemic to Northern Madagascar. We focused on the population of M. tavaratra in the Loky–Manambato region, Northern Madagascar, a region delimited by two permanent rivers and characterized by a mosaic of fragmented forests. We genotyped 148 individuals at three mitochondrial loci (D-loop, cytb, and cox2) in all the major forests of the study region. Our analyses suggest that M. tavaratra holds average genetic diversity when compared to other mouse lemur species, and we identified two to four genetic clusters in the study region, a pattern similar to that observed in another lemur endemic to the region (Propithecus tattersalli). The main cluster involved samples from the two mountain forests in the study region, which were connected until recently. However, the river crossing the study region does not appear to be a strict barrier to gene flow in M. tavaratra. Finally, the inferred demographic history of M. tavaratra suggests no detectable departure from stationarity over the last millennia. Comparisons with codistributed species (P. tattersalli and two endemic rodents, Eliurus spp.) suggest both differences and similarities in the genetic clusters identified (i.e., barriers to species dispersal) and in the inferred demographic history. These comparisons suggest that studies of codistributed species are important to understand the effects of landscape features on species and to reconstruct the history of habitat changes in a region.