Genetic diversity in butterflies: Interactive effects of habitat fragmentation and climate-driven range expansion

Some species are expanding their ranges polewards during current climate warming. However, anthropogenic fragmentation of suitable habitat is affecting expansion rates and here we investigate interactions between range expansion, habitat fragmentation and genetic diversity. We examined three closely related Satyrinae butterflies, which differ in their habitat associations, from six sites along a transect in England from distribution core to expanding range margin. There was a significant decline in allozyme variation towards an expanding range margin in Pararge aegeria, which has the most restricted habitat availability, but not in Pyronia tithonus whose habitat is more widely available, or in a non-expanding 'control species' (Maniola jurtina). Moreover, data from another transect in Scotland indicated that declines in genetic diversity in P. aegeria were evident only on the transect in England, which had greater habitat fragmentation. Our results indicate that fragmentation of breeding habitats leads to more severe founder events during colonization, resulting in reduced diversity in marginal populations in more specialist species. The continued widespread loss of suitable habitats in the future may increase the likelihood of loss of genetic diversity in expanding species, which may affect whether or not species can adapt to future environmental change.     

Community structure in temporary freshwater pools: disentangling the effects of habitat size and hydroregime

1. Hydroregime (duration, frequency and predictability of the aquatic phase) is a key feature of temporary aquatic habitats that not only moulds community structure and diversity (species sorting) but also life history characteristics of the inhabitants (natural selection). However, since hydroregime is a complex multidimensional entity that cannot be estimated from short term observations, morphometric variables are commonly used as proxies for hydroregime, making it impossible to separate effects of habitat size and hydroregime on biota.
2. We have used a simple hydrological model, validated with recent (average r ² = 96%) and historic water level observations (average r ² = 81%), to accurately reconstruct hydroregime based on historical rainfall and evaporation data in a cluster of 36 temporary rock pools in central South Africa.
3. Using the model output, we demonstrated that both hydroregime and habitat size had unique and shared effects on temporary pool biota and that these effects depended on the dispersal modes of the taxa. Model-generated hydrological data explained more variation in community patterns than short-term observations of hydroperiod. Hydroregime was more important for passive dispersers than for active dispersers that can migrate when pools dry up. Basin morphometry was a relatively poor predictor of pool hydroregime. We concluded that simple modelling may greatly improve the resolution of studies linking hydroregime to biological variables.
4. An accurate account of hydrological variation provides a firm foundation to understand community and population structure and dynamics in temporary aquatic habitats. Since many of these habitats have been destroyed or degraded in recent decades, our findings and tools may contribute to the development of reliable conservation guidelines.     

Predator effects on aquatic community assembly: disentangling the roles of habitat selection and post-colonization processes

Top predators are known to play an important role in the assembly of communities via two mechanisms: (1) by altering the colonization (or emigration) patterns of prey through behavioral habitat selection, and (2) by altering vital rates (e.g. mortality, birth) of prey after colonization. While both these mechanisms act to determine assembly, research has focused on either their combined overall effects (confounding them), or examined them singly. As a result, it remains unclear how these mechanisms act to sequentially shape community structure. In this study, we experimentally disentangle habitat selection and post‐colonization effects of predaceous fish to test their independent and combined influence on the assembly of insect and larval amphibian communities in experimental freshwater habitats. Specifically, we ask, ‘do the behavioral choices of colonists continue to structure aquatic communities even after post‐colonization processes have occurred?’ Like previous studies, we found that colonization was strongly reduced by the presence of fish cues. More importantly, these effects of fish on prey colonization behavior combined independently with post‐colonization processes to determine the overall effect of predators on community assembly. Although habitat selection and predation both reduced abundance and biomass of most taxa in the post‐colonization communities, these factors had qualitatively different effects on aspects of trophic structure. Habitat selection altered the ratio of secondary to primary consumer abundance and biomass, while post‐colonization predation drove strong trophic cascades not observed in response to habitat selection. Our results suggest that behavioral choices regarding habitat selection can have lasting and unique effects on the structure of aquatic communities.     

Changes in climate and habitat suitability for the cattle tick Boophilus microplus in its southern Neotropical distribution range.

We addressed the possible effects of several climate scenarios on habitat suitability (HS) for the cattle tick Boophilus microplus and the probability of producing permanent populations from introduced females of that tick in central parts of Argentina, using both a correlative model (derived from climate predictors) and a mechanistic (life cycle) model. There was high correlation (R2 = 0.866) between HS-derived and life cycle outputs for HS values higher than 0.52, suggesting that HS is a good estimator of the life cycle of the tick above a critical threshold of HS values. Scenarios with increased temperatures increased suitable habitats for the tick in southern parts of the study region, extending below parallel 34 degrees S, but suitable habitats remained limited in the west. A concurrent increase in rainfall produced a further increase of HS in these areas. Results from the life cycle model suggest that in areas of suitable habitat, permanent cattle tick populations are most probable if engorged females are introduced during mid-summer.     

Modelling the effect of habitat fragmentation on range expansion in a butterfly

There is an increasing need for conservation programmes to make quantitative predictions of biodiversity responses to changed environments. Such predictions will be particularly important to promote species recovery in fragmented landscapes, and to understand and facilitate distribution responses to climate change. Here, we model expansion rates of a test species (a rare butterfly, Hesperia comma) in five landscapes over 18 years (generations), using a metapopulation model (the incidence function model). Expansion rates increased with the area, quality and proximity of habitat patches available for colonization, with predicted expansion rates closely matching observed rates in test landscapes. Habitat fragmentation constrained expansion, but in a predictable way, suggesting that it will prove feasible both to understand variation in expansion rates and to develop conservation programmes to increase rates of range expansion in such species.     

Serial founder effects during range expansion: a spatial analog of genetic drift

Range expansions cause a series of founder events. We show that, in a one-dimensional habitat, these founder events are the spatial analog of genetic drift in a randomly mating population. The spatial series of allele frequencies created by successive founder events is equivalent to the time series of allele frequencies in a population of effective size ke, the effective number of founders. We derive an expression for ke in a discrete-population model that allows for local population growth and migration among established populations. If there is selection, the net effect is determined approximately by the product of the selection coefficients and the number of generations between successive founding events. We use the model of a single population to compute analytically several quantities for an allele present in the source population: (i) the probability that it survives the series of colonization events, (ii) the probability that it reaches a specified threshold frequency in the last population, and (iii) the mean and variance of the frequencies in each population. We show that the analytic theory provides a good approximation to simulation results. A consequence of our approximation is that the average heterozygosity of neutral alleles decreases by a factor of 1-1/(2ke) in each new population. Therefore, the population genetic consequences of surfing can be predicted approximately by the effective number of founders and the effective selection coefficients, even in the presence of migration among populations. We also show that our analytic results are applicable to a model of range expansion in a continuously distributed population.     

Linking habitat use to range expansion rates in fragmented landscapes: a metapopulation approach

Temperature increases because of climate change are expected to cause expansions at the high latitude margins of species distributions, but, in practice, fragmented landscapes act as barriers to colonization for most species. Understanding how species distributions will shift in response to climate change therefore requires techniques that incorporate the combined effects of climate and landscape‐scale habitat availability on colonization rates. We use a metapopulation model (Incidence Function Model, IFM) to test effects of fine‐scale habitat use on patterns and rates of range expansion by the butterfly Hesperia comma. At its northern range margin in Britain, this species has increased its breadth of microhabitat use because of climate warming, leading to increased colonization rates. We validated the IFM by reconstructing expansions in five habitat networks between 1982 and 2000, before using it to predict metapopulation dynamics over 100 yr, for three scenarios based on observed changes to habitat use. We define the scenarios as “cold‐world” (only hot, south‐facing 150–250° hillsides are deemed warm enough), “warm‐world” in which 100–300° hillsides can be populated, and “hot‐world”, where the background climate is warm enough to enable use of all aspects (as increasingly observed). In the simulations, increased habitat availability in the hot‐world scenario led to faster range expansion rates, and to long‐term differences in distribution size and pattern. Thus, fine‐scale changes in the distribution of suitable microclimates led to landscape‐scale changes in population size and colonization rate, resulting in coarse‐scale changes to the species distribution. Despite use of a wider range of habitats associated with climate change, H. comma is still expected to occupy a small fraction of available habitat in 100 yr. The research shows that metapopulation models represent a potential framework to identify barriers to range expansion, and to predict the effects of environmental change or conservation interventions on species distributions and persistence.     

Relationships of climate,residence time,and biogeographical origin with the range sizes and species richness patterns of exotic plants in Great Britain

Based on atlas data with a 10-km cell resolution for 1,406 exotic plant species inhabiting Great Britain, we investigate the extent to which arrival time (residence time) and biogeographical origin (climate suitability) are associated with range sizes of exotic plants and how exotic plant richness is related to current climate and the human footprint. We grouped species according to four arrival periods (archaeophytes and three classes of neophytes), and three broad biogeographical origins, each reflecting a different macroclimate similarity with the study region (northern Holarctic > Mediterranean > and tropical–subtropical). While we found that mean range sizes increased with residence time, no strong effect of the region of origin on range size was detected. Also, across all groups, species richness was primarily and positively associated with temperature, whereas relationships with human footprint were much weaker, albeit also positive in all cases. The proportion of variance explained by environmental models of richness increased from groups comprising recently arrived species to those that arrived earlier, and from tropical–subtropical species to exotics coming from the Holarctic. Our data also illustrate how these trends translate into richness patterns and their association with climate, which become more similar to native richness patterns as residence time and macroclimatic matching increase. In contrast, broad-scale human alteration of ecosystems appeared to be less important for variation in exotic richness than climate, although we did not evaluate anthropogenic effects at finer scales.     

Serial founder effects and genetic differentiation during worldwide range expansion of monarch butterflies

Range expansions can result in founder effects, increasing genetic differentiation between expanding populations and reducing genetic diversity along the expansion front. However, few studies have addressed these effects in long-distance migratory species, for which high dispersal ability might counter the effects of genetic drift. Monarchs (Danaus plexippus) are best known for undertaking a long-distance annual migration in North America, but have also dispersed around the world to form populations that do not migrate or travel only short distances. Here, we used microsatellite markers to assess genetic differentiation among 18 monarch populations and to determine worldwide colonization routes. Our results indicate that North American monarch populations connected by land show limited differentiation, probably because of the monarch''s ability to migrate long distances. Conversely, we found high genetic differentiation between populations separated by large bodies of water. Moreover, we show evidence for serial founder effects across the Pacific, suggesting stepwise dispersal from a North American origin. These findings demonstrate that genetic drift played a major role in shaping allele frequencies and created genetic differentiation among newly formed populations. Thus, range expansion can give rise to genetic differentiation and declines in genetic diversity, even in highly mobile species.     

Invasive birds in a novel landscape: habitat associations and effects on established species

Studying the relationships among introduced species, their preferred habitats, and native species can be important for predicting the effects of invasions on native populations. Examining the colonization of North America by the Eurasian collared‐dove Streptopelia decaocto, we quantified the habitat characteristics of sites most likely to be occupied by this invasive bird species in the early stages of the invasion. Further, we studied the relationship between collared‐dove abundance and the abundance of other dove species in the study area, anticipating a negative effect on established species following the introduction of a potential competitor. Linking satellite‐derived landcover data with winter bird community data gathered from 444 study sites in Florida, USA from 1999 to 2008, we found that collared‐doves were more likely to occur in landscapes that had been highly‐modified by human activity than in forested landscapes. Collared‐dove abundance increased as the proportion of the landscape characterized as low‐intensity development and medium/high‐intensity development increased. The probability of collared‐doves occurring at a site was also related to the spatial proximity of other sites reporting doves (positive spatial autocorrelation). Contrary to our expectations, the site‐level abundance of four other dove species all increased with collared‐dove abundance throughout the sampling period. Interactions between collared‐doves and native species should be further studied in different environments as this invasive bird rapidly colonizes North America.     

North American Brant: effects of changes in habitat and climate on population dynamics

We describe the importance of key habitats used by four nesting populations of nearctic brant (Branta bernicla) and discuss the potential relationship between changes in these habitats and population dynamics of brant. Nearctic brant, in contrast to most geese, rely on marine habitats and native intertidal plants during the non‐breeding season, particularly the seagrass, Zostera, and the macroalgae, Ulva. Atlantic and Eastern High Arctic brant have experienced the greatest degradation of their winter habitats (northeastern United States and Ireland, respectively) and have also shown the most plasticity in feeding behavior. Black and Western High Arctic brant of the Pacific Flyway are the most dependent on Zostera, and are undergoing a shift in winter distribution that is likely related to climate change and its associated effects on Zostera dynamics. Variation in breeding propensity of Black Brant associated with winter location and climate strongly suggests that food abundance on the wintering grounds directly affects reproductive performance in these geese. In summer, salt marshes, especially those containing Carex and Puccinellia, are key habitats for raising young, while lake shorelines with fine freshwater grasses and sedges are important for molting birds. Availability and abundance of salt marshes has a direct effect on growth and recruitment of goslings and ultimately, plays an important role in regulating size of local brant populations.     

Contrasting effects of long distance seed dispersal on genetic diversity during range expansion

Currently many attempts are made to reconstruct the colonization history of plant species after the last ice age. A surprising finding is that during the colonization phase genetic diversity did not decrease as much as expected. In this paper we examine whether long distance seed dispersal events could play a role in the unexpected maintenance of genetic diversity during range expansion. This study is based on simulations carried out with a maternally inherited haploid locus using a cellular automaton. The simulations reveal a close relationship between the frequency of long distance seed dispersal events and the amount of genetic diversity preserved during colonization. In particular, when the colonized region is narrow, a complete loss of genetic diversity results from the occurrence of very rare long distance dispersal (LDD) events. We call this phenomenon the 'embolism effect'. However, slightly higher rates of LDD events reverse this effect, up to the point that diversity is better preserved than in a pure diffusion model. This phenomenon is linked to the reorganization of the genetic structure during colonization and is called the 'reshuffling effect'.     

Impacts of climate warming and habitat loss on extinctions at species' low-latitude range boundaries

Polewards expansions of species' distributions have been attributed to climate warming, but evidence for climate‐driven local extinctions at warm (low latitude/elevation) boundaries is equivocal. We surveyed the four species of butterflies that reach their southern limits in Britain. We visited 421 sites where the species had been recorded previously to determine whether recent extinctions were primarily due to climate or habitat changes. Coenonympha tullia had become extinct at 52% of study sites and all losses were associated with habitat degradation. Aricia artaxerxes was extinct from 50% of sites, with approximately one‐third to half of extinctions associated with climate‐related factors and the remainder with habitat loss. For Erebia aethiops (extinct from 24% of sites), approximately a quarter of the extinctions were associated with habitat and three‐quarters with climate. For Erebia epiphron, extinctions (37% of sites) were attributed mainly to climate with almost no habitat effects. For the three species affected by climate, range boundaries retracted 70–100 km northwards (A. artaxerxes, E. aethiops) and 130–150 m uphill (E. epiphron) in the sample of sites analysed. These shifts are consistent with estimated latitudinal and elevational temperature shifts of 88 km northwards and 98 m uphill over the 19‐year study period. These results suggest that the southern/warm range margins of some species are as sensitive to climate change as are northern/cool margins. Our data indicate that climate warming has been of comparable importance to habitat loss in driving local extinctions of northern species over the past few decades; future climate warming is likely to jeopardize the long‐term survival of many northern and mountain species.     

Reid's paradox revisited: the evolution of dispersal kernels during range expansion

Current approaches to modeling range advance assume that the distribution describing dispersal distances in the population (the "dispersal kernel") is a static entity. We argue here that dispersal kernels are in fact highly dynamic during periods of range advance because density effects and spatial assortment by dispersal ability ("spatial selection") drive the evolution of increased dispersal on the expanding front. Using a spatially explicit individual-based model, we demonstrate this effect under a wide variety of population growth rates and dispersal costs. We then test the possibility of an evolved shift in dispersal kernels by measuring dispersal rates in individual cane toads (Bufo marinus) from invasive populations in Australia (historically, toads advanced their range at 10 km/year, but now they achieve >55 km/year in the northern part of their range). Under a common-garden design, we found a steady increase in dispersal tendency with distance from the invasion origin. Dispersal kernels on the invading front were less kurtotic and less skewed than those from origin populations. Thus, toads have increased their rate of range expansion partly through increased dispersal on the expanding front. For accurate long-range forecasts of range advance, we need to take into account the potential for dispersal kernels to be evolutionarily dynamic.     

Coexistence of individual and social learners during range expansion

Individual learning and social learning are two primary abilities supporting cultural evolution. Conditions for their evolution have mostly been studied by investigating gene frequency dynamics, which essentially implies constant population size. Predictions from such “static” models may only be of partial relevance to the evolution of advanced individual learning in modern humans, because modern humans have experienced rapid population growth and range expansion during “out-of-Africa.” Here we model the spatial population dynamics of individual and social learners by a reaction–diffusion system. One feature of our model is the inclusion of the possibility that social learners may fail to find an exemplar to copy in regions where the population density is low. Due to this attenuation effect, the invasion speed of social learners is diminished, and various kinds of invasion dynamics are observed. Our primary findings are: (1) individual learners can persist indefinitely when invading environmentally homogeneous infinite space; (2) the occurrence of individual learners at the front may inhibit the spread of social learners. These results suggest that “out-of-Africa” may have driven the evolution of advanced individual learning ability in modern humans.     

Future coral reef habitat marginality: temporal and spatial effects of climate change in the Pacific basin

Marginal reef habitats are regarded as regions where coral reefs and coral communities reflect the effects of steady-state or long-term average environmental limitations. We used classifications based on this concept with predicted time-variant conditions of future climate to develop a scenario for the evolution of future marginality. Model results based on a conservative scenario of atmospheric CO₂ increase were used to examine changes in sea surface temperature and aragonite saturation state over the Pacific Ocean basin until 2069. Results of the projections indicated that essentially all reef locations are likely to become marginal with respect to aragonite saturation state. Significant areas, including some with the highest biodiversity, are expected to experience high-temperature regimes that may be marginal, and additional areas will enter the borderline high temperature range that have experienced significant ENSO-related bleaching in the recent past. The positive effects of warming in areas that are presently marginal in terms of low temperature were limited. Conditions of the late 21st century do not lie outside the ranges in which present-day marginal reef systems occur. Adaptive and acclimative capabilities of organisms and communities will be critical in determining the future of coral reef ecosystems.Electronic supplementary material is available for this article if you access the article at . A link in the frame on the left on that page takes you directly to the supplementary material.     

Multiple habitat associations: the role of offsite habitat in determining onsite avian density and species richness

Many animal populations continue to decline despite occurring in protected areas or on sympathetically managed sites. Frequently, this is because a specific habitat patch may not fulfil all the niche requirements of a threatened species. For instance, species often move between, and make use of, multiple habitat types for breeding, roosting and feeding within the same landscape. These cross‐habitat interactions present a challenge for conservation. Here we quantify how the habitat associations of individual species and assemblages occurring within two distinct but adjacent habitat types (moorland and farmland) determine a suite of density and richness indicators, using the bird community of the English uplands as a case study. There was a clear association between onsite avian density and richness and offsite habitat structure (e.g. vegetation height, percent cover of dominant plant species, land management practices). Although such effects are not universal across all species and assemblages, where present (for five farmland and three moorland indicators) the increase in explanatory power offered by including offsite habitat structure can be large. By constructing scenarios of possible changes to management practice on both moorland and farmland, we demonstrate a real conservation benefit can be obtained by altering management in offsite habitats. For example, reducing burning intensity on moorland can result in a five‐fold increase in snipe Gallinago gallinago density on farmland, without an alteration in farmland habitat. For one species (Eurasian curlew Numenius arquata), we demonstrate the frequency with which birds move between and utilise farmland and moorland during the breeding season, and therefore the importance of both habitat types to maintaining population densities. The multiple habitat dependency phenomenon quantified here is common and not restricted to birds. The successful conservation of many threatened species will thus depend on coordinated cross‐habitat management.     

Changes in dispersal during species' range expansions

Explanations for rapid species' range expansions have typically been purely ecological, with little attention given to evolutionary processes. We tested predictions for the evolution of dispersal during range expansion using four species of wing-dimorphic bush cricket (Conocephalus discolor, Conocephalus dorsalis, Metrioptera roeselii, and Metrioptera brachyptera). We observed distinct changes in dispersal in the two species with expanding ranges. Recently colonized populations at the range margin showed increased frequencies of dispersive, long-winged (macropterous) individuals, compared with longer-established populations in the range core. This increase in dispersal appeared to be short-lived because 5-10 years after colonization populations showed similar incidences of macroptery to populations in the range core. These changes are consistent with evolutionary change; field patterns persisted when nymphs were reared under controlled environmental conditions, and range margin individuals reared in the laboratory flew farther than range core individuals in a wind tunnel. There was also a reproductive trade-off with dispersal in both females and males, which could explain the rapid reversion to lower rates of dispersal once populations become established. The effect of population density on wing morphology differed between populations from the range core (no significant effect of density) and expanding range margins (negative density dependence), which we propose is part of the mechanism of the changes in dispersal. Transient changes in dispersal are likely to be common in many species undergoing range expansion and can have major population and biogeographic consequences.