Northern range expansion of European populations of the wasp spider Argiope bruennichi is associated with global warming–correlated genetic admixture and population‐specific temperature adaptations

Poleward range expansions are observed for an increasing number of species, which may be an effect of global warming during the past decades. However, it is still not clear in how far these expansions reflect simple geographical shifts of species ranges, or whether new genetic adaptations play a role as well. Here, we analyse the expansion of the wasp spider Argiope bruennichi into Northern Europe during the last century. We have used a range‐wide sampling of contemporary populations and historical specimens from museums to trace the phylogeography and genetic changes associated with the range shift. Based on the analysis of mitochondrial, microsatellite and SNP markers, we observe a higher level of genetic diversity in the expanding populations, apparently due to admixture of formerly isolated lineages. Using reciprocal transplant experiments for testing overwintering tolerance, as well as temperature preference and tolerance tests in the laboratory, we find that the invading spiders have possibly shifted their temperature niche. This may be a key adaptation for survival in Northern latitudes. The museum samples allow a reconstruction of the invasion's genetic history. A first, small‐scale range shift started around 1930, in parallel with the onset of global warming. A more massive invasion of Northern Europe associated with genetic admixture and morphological changes occurred in later decades. We suggest that the latter range expansion into far Northern latitudes may be a consequence of the admixture that provided the genetic material for adaptations to new environmental regimes. Hence, global warming could have facilitated the initial admixture of populations and this resulted in genetic lineages with new habitat preferences.     

Neutral and adaptive genomic signatures of rapid poleward range expansion

Many species are expanding their range polewards, and this has been associated with rapid phenotypic change. Yet, it is unclear to what extent this reflects rapid genetic adaptation or neutral processes associated with range expansion, or selection linked to the new thermal conditions encountered. To disentangle these alternatives, we studied the genomic signature of range expansion in the damselfly Coenagrion scitulum using 4950 newly developed genomic SNPs and linked this to the rapidly evolved phenotypic differences between core and (newly established) edge populations. Most edge populations were genetically clearly differentiated from the core populations and all were differentiated from each other indicating independent range expansion events. In addition, evidence for genetic drift in the edge populations, and strong evidence for adaptive genetic variation in association with the range expansion was detected. We identified one SNP under consistent selection in four of the five edge populations and showed that the allele increasing in frequency is associated with increased flight performance. This indicates collateral, non‐neutral evolutionary changes in independent edge populations driven by the range expansion process. We also detected a genomic signature of adaptation to the newly encountered thermal regimes, reflecting a pattern of countergradient variation. The latter signature was identified at a single SNP as well as in a set of covarying SNPs using a polygenic multilocus approach to detect selection. Overall, this study highlights how a strategic geographic sampling design and the integration of genomic, phenotypic and environmental data can identify and disentangle the neutral and adaptive processes that are simultaneously operating during range expansions.     

Winter climate change and the poleward range expansion of a tropical invasive tree (Brazilian pepper—Schinus terebinthifolius)

Winter climate change is expected to lead to the tropicalization of temperate ecosystems, where tropical species expand poleward in response to a decrease in the intensity and duration of winter temperature extremes (i.e., freeze events). In the southeastern United States, freezing temperatures control the northern range limits of many invasive nonnative species. Here, we examine the influence of freezing temperatures and winter climate change on the northern range limits of an invasive nonnative tree—Schinus terebinthifolius (Brazilian pepper). Since introduction in the 1800s, Brazilian pepper has invaded ecosystems throughout south and central Florida to become the state's most widespread nonnative plant species. Although Brazilian pepper is sensitive to freezing temperatures, temperature controls on its northern distribution have not been adequately quantified. We used temperature and plant occurrence data to quantify the sensitivity of Brazilian pepper to freezing temperatures. Then, we examined the potential for range expansion under three alternative future climate scenarios (+2°C, +4°C, and +6°C). Our analyses identify a strong nonlinear sigmoidal relationship between minimum temperature and Brazilian pepper presence, with a discrete threshold temperature occurring near ?11°C. Our future scenario analyses indicate that, in response to warming winter temperatures, Brazilian pepper is expected to expand northward and transform ecosystems in north Florida and across much of the Gulf of Mexico and south Atlantic coasts of the United States. These results underscore the importance of early detection and rapid response efforts to identify and manage the northward invasion of Brazilian pepper in response to climate change. Looking more broadly, our work highlights the need to anticipate and prepare for the tropicalization of temperate ecosystems by tropical invasive species.     

Organization of the spinnerets and spigots in the orb web spider,Argiope bruennichi (Araneae: Araneidae)

Although the basic taxonomic characteristics usually remain unchanged, some spinning apparatuses undergo consistent adaptive variations. As the presence of additional protuberances known as nubbins and tartipores have caused disagreements regarding some Araneidae spiders, more detailed definitions on the cuticular structures have recently been proposed. Reflecting this definition, microstructural organization of silk spinning apparatuses in the orb web spider Argiope bruennichi were reconsidered using field emission scanning electron microscopy. Among the seven kinds of functional spigots in females, it was revealed that two types (major ampullates and pyrifoms) are located on anterior spinnerets and another five types are distributed on median (minor ampullates, tubuliforms and aciniforms) or posterior (tubuliforms, flagelliforms, aggregates and aciniforms) spinnerets, respectively. In addition to functional spigots, cuticular remnants of the nubbins and the tartipores were found on the spinning fields, but the number of tartipores on each spinneret varied among individuals based on maturity. Nevertheless, three kinds of cuticular protuberances of ampullate silk glands were clearly visible at both the anterior and median spinnerets.     

Long‐distance dispersal maximizes evolutionary potential during rapid geographic range expansion

Conventional wisdom predicts that sequential founder events will cause genetic diversity to erode in species with expanding geographic ranges, limiting evolutionary potential at the range margin. Here, we show that invasive European starlings (Sturnus vulgaris) in South Africa preserve genetic diversity during range expansion, possibly as a result of frequent long‐distance dispersal events. We further show that unfavourable environmental conditions trigger enhanced dispersal, as indicated by signatures of selection detected across the expanding range. This brings genetic variation to the expansion front, counterbalancing the cumulative effects of sequential founding events and optimizing standing genetic diversity and thus evolutionary potential at range margins during spread. Therefore, dispersal strategies should be highlighted as key determinants of the ecological and evolutionary performances of species in novel environments and in response to global environmental change.     

Plant–soil interactions in the expansion and native range of a poleward shifting plant species

Climate warming causes range shifts of many species toward higher latitudes and altitudes. However, range shifts of host species do not necessarily proceed at the same rates as those of their enemies and symbionts. Here, we examined how a range shifting plant species performs in soil from its original range in comparison with soil from the expansion range. Tragopogon dubius is currently expanding from southern into north-western Europe and we examined how this plant species responds to soil communities from its original and expansion ranges. We compared the performance of T. dubius with that of the closely related Tragopogon pratensis , which has a natural occurrence along the entire latitudinal gradient. Inoculation with the rhizosphere soil from T. dubius populations of the original range had a more negative effect on plant biomass production than inoculation with rhizosphere soil from the expansion range. Interestingly, the nonrange expander T. pratensis experienced a net negative soil effect throughout this entire range. The effects observed in this species pair may be due to release from soil born enemies or accumulation of beneficial soil born organisms. If this phenomenon applies broadly to other species, then range expansion may enable plants species to show enhanced performance.     

Different positions of males approaching towards females and male choices between webs with and without stabilimentum in a sexually cannibalistic orb‐web spider,Argiope bruennichi

Males of the orb‐weaving spider species Argiope bruennichi (Araneidae) are frequently victims of sexual cannibalism. Therefore, a male spider approaching a female should have strategies to avoid being killed before copulation. Our present field study detected six types of A. bruennichi male positions vis‐à‐vis the female web. In 78% of situations (39/50), only one male attached to a female. Two males attached to the same female in 11 cases. We observed no cases of three or more males on the same female web. We most commonly observed the situation of a male staying in its own web and connecting to a female's web with its silk thread (46% of cases). Of the female webs chosen by males, 68% were decorated with both an upper and lower portion of stabilimentum – a conspicuous white silk structure that reflects much more ultraviolet light than other spider silks in the web. Only 14% (7/50) of the selected webs lacked stabilimentum. Therefore, we conducted an experiment to investigate the males' choice between females' webs with and without stabilimentum. Of the 24 males used in the experiment, 10 chose webs with stabilimentum. This result did not show a strong preference of the male for stabilimentum between equally sized webs, and thus did not support an earlier suggestion that stabilimentum in A. bruennichi might function to guide males to females for mating.     

Temperature‐related geographical shifts among passerines: contrasting processes along poleward and equatorward range margins

Climate change is causing widespread geographical range shifts, which likely reflects different processes at leading and trailing range margins. Progressive warming is thought to relax thermal barriers at poleward range margins, enabling colonization of novel areas, but imposes increasingly unsuitable thermal conditions at equatorward margins, leading to range losses from those areas. Few tests of this process during recent climate change have been possible, but understanding determinants of species’ range limits will improve predictions of their geographical responses to climate change and variation in extinction risk. Here, we examine the relationship between poleward and equatorward range margin dynamics with respect to temperature‐related geographical limits observed for 34 breeding passerine species in North America between 1984–1988 and 2002–2006. We find that species’ equatorward range margins were closer to their upper realized thermal niche limits and proximity to those limits predicts equatorward population extinction risk through time. Conversely, the difference between breeding bird species’ poleward range margin temperatures and the coolest temperatures they tolerate elsewhere in their ranges was substantial and remained consistent through time: range expansion at species’ poleward range margins is unlikely to directly reflect lowered thermal barriers to colonization. The process of range expansion may reflect more complex factors operating across broader areas of species’ ranges. The latitudinal extent of breeding bird ranges is decreasing through time. Disparate responses observed at poleward versus equatorward margins arise due to differences in range margin placement within the realized thermal niche and suggest that climate‐induced geographical shift at equatorward range limits more strongly reflect abiotic conditions than at their poleward range limits. This further suggests that observed geographic responses to date may fail to demonstrate the true cost of climate change on the poleward portion of species’ distributions. Poleward range margins for North American breeding passerines are not presently in equilibrium with realized thermal limits.     

The genetic signature of rapid range expansion by flying squirrels in response to contemporary climate warming

Climate is an important factor limiting species distributions. Historic climate‐change related range movements have modified the genetic diversity of species by the merging and splitting of gene pools and by the effects associated with recurrent founder events. These effects are often inferred, either from retrospective analyses of current genetic patterns or from simulations. Rarely has it been possible for the population genetic effects of range expansion to be examined with contemporaneous demographic data. We characterized the genetic signature of rapid range expansion by southern flying squirrels (Glaucomys volans) and compared these results to a stationary population of the closely related northern flying squirrel (Glaucomys sabrinus) in Ontario, Canada. Samples were taken during an approximately 200 km range expansion by G. volans (1994–2003) and genotyped at 6 (G. sabrinus) and 8 (G. volans) microsatellite loci. For G. volans, but not G. sabrinus, we found evidence of a latitudinal gradient in allele frequencies and a decrease in allelic richness along the axis of expansion. We found no evidence of isolation‐by‐distance in either species or of genetic bottlenecks in the area of G. volans expansion. These results suggest that serial founder events can cause an immediate reduction in genetic diversity following rapid range expansion with high levels of gene flow giving rise to heterogeneity within what would classically be termed panmixia. Given the pace of anthropogenic climate change, and the increasing incidence of range movements in response, this may be an important, immediate consequence of climate change.     

Population genetic analysis of a recent range expansion: mechanisms regulating the poleward range limit in the volcano barnacle Tetraclita rubescens

As range shifts coincident with climate change have become increasingly well documented, efforts to describe the causes of range boundaries have increased. Three mechanisms—genetic impoverishment, migration load, or a physical barrier to dispersal—are well described theoretically, but the data needed to distinguish among them have rarely been collected. We describe the distribution, abundance, genetic variation, and environment of Tetraclita rubescens, an intertidal barnacle that expanded its northern range limit by several hundreds of kilometres from San Francisco, CA, USA, since the 1970s. We compare geographic variation in abundance with abiotic and biotic patterns, including sea surface temperatures and the distributions of 387 co‐occurring species, and describe genetic variation in cytochrome c oxidase subunit I, mitochondrial noncoding region, and nine microsatellite loci from 27 locations between Bahia Magdalena (California Baja Sur, Mexico) and Cape Mendocino (CA, USA). We find very high gene flow, high genetic diversity, and a gradient in physical environmental variation coincident with the range limit. We infer that the primary cause of the northern range boundary in T. rubescens is migration load arising from flow of maladapted alleles into peripheral locations and that environmental change, which could have reduced selection against genotypes immigrating into the newly colonized portion of the range, is the most likely cause of the observed range expansion. Because environmental change could similarly affect all taxa in a region whose distributional limits are established by migration load, these mechanisms may be common causes of range boundaries and largely synchronous multi‐species range expansions.     

Effects of social information on life history and mating tactics of males in the orb‐web spider Argiope bruennichi

Informed mating decisions are often based on social cues providing information about prospective mating opportunities. Social information early in life can trigger developmental modifications and influence later mating decisions. A high adaptive value of such adjustments is particularly obvious in systems where potential mating rates are extremely limited and have to be carried out in a short time window. Males of the sexually cannibalistic spider Argiope bruennichi can achieve maximally two copulations which they can use for one (monogyny) or two females (bigyny). The choice between these male mating tactics should rely on female availability that males might assess through volatile sex pheromones emitted by virgin females. We predict that in response to those female cues, males of A. bruennichi should mature earlier and at a smaller body size and favor a bigynous mating tactic in comparison with controls. We sampled spiders from two areas close to the Southern and Northern species range to account for differences in mate quality and seasonality. In a fully factorial design, half of the subadult males from both areas obtained silk cues of females, while the other half remained without female exposure. Adult males were subjected to no‐choice mating tests and could either monopolize the female or leave her (bigyny). We found that Southern males matured later and at a larger size than Northern males. Regardless of their origin, males also shortened the subadult stage in response to female cues, which, however, had no effects on male body mass. Contrary to our prediction, the frequencies of mating tactics were unaffected by the treatment. We conclude that while social cues during late development elicit adaptive life history adjustments, they are less important for the adjustment of mating decisions. We suggest that male tactics mostly rely on local information at the time of mate search.     

Inferring the geographic origin of a range expansion: Latitudinal and longitudinal coordinates inferred from genomic data in an ABC framework with the program x‐origin

Climatic or environmental change is not only driving distributional shifts in species today, but it has also caused distributions to expand and contract in the past. Inferences about the geographic locations of past populations especially regions that served as refugia (i.e., source populations) and migratory routes are a challenging endeavour. Refugial areas may be evidenced from fossil records or regions of temporal stability inferred from ecological niche models. Genomic data offer an alternative and broadly applicable source of information about the locality of refugial areas, especially relative to fossil data, which are either unavailable or incomplete for most species. Here, we present a pipeline we developed (called x ‐origin ) for statistically inferring the geographic origin of range expansion using a spatially explicit coalescent model and an approximate Bayesian computation testing framework. In addition to assessing the probability of specific latitudinal and longitudinal coordinates of refugial or source populations, such inferences can also be made accounting for the effects of temporal and spatial environmental heterogeneity, which may impact migration routes. We demonstrate x ‐origin with an analysis of genomic data collected in the Collared pika that underwent postglacial expansion across Alaska, as well as present an assessment of its accuracy under a known model of expansion to validate the approach.     

Deforestation and cattle ranching drive rapid range expansion of capybara in the Gran Chaco ecosystem

Anthropogenic habitat alteration has the capacity to alter the distribution of species. Capybara (Hydrochoerus hydrochaeris) are a widely distributed rodent throughout most of South America, but are restricted to areas of standing water. As the Gran Chaco ecosystem of Paraguay is converted from dry tropical forest to pastureland, we hypothesize that this alteration creates potential for invasion by capybara into newly fragmented areas. We surveyed throughout the Chaco to estimate the distribution of capybara, and we collected noninvasive genetic samples. We used ecological niche modeling based on six environmental or climatic variables, and we modeled both the current distribution of capybara and the distribution of capybara 80 years ago. We then verified the hypothesized demographic signal generated with our model using phylogeographic analyses of 386 bp of the mtDNA control region. Comparison of present and past models suggested that populations expanded into the Gran Chaco after forest was converted to pastureland. Analyses of the mitochondrial D‐loop supported the rapid range expansion scenario. We also found evidence of secondary contact of two distinct phylogroups which had previously been disjunct. Anthropogenic land transformation appeared to be a major factor influencing the distribution, as predicted by the niche model and confirmed by genetic data. Habitat modification altered connectivity of populations across the landscape. In addition, long separated clades of capybara are now admixed throughout the Paraguayan Chaco. The invasion of a large bodied herbivore into the High Chaco region may exacerbate the degradation of forest and prevent forest regeneration. As the reservoir host of several zoonotic diseases, the expansion and contact of two previously disjunct capybara populations has implications for disease emergence.     

Annual temperature variation as a time machine to understand the effects of long‐term climate change on a poleward range shift

Range shifts due to annual variation in temperature are more tractable than range shifts linked to decadal to century long temperature changes due to climate change, providing natural experiments to determine the mechanisms responsible for driving long‐term distributional shifts. In this study we couple physiologically grounded mechanistic models with biogeographic surveys in 2 years with high levels of annual temperature variation to disentangle the drivers of a historical range shift driven by climate change. The distribution of the barnacle Semibalanus balanoides has shifted 350 km poleward in the past half century along the east coast of the United States. Recruits were present throughout the historical range following the 2015 reproductive season, when temperatures were similar to those in the past century, and absent following the 2016 reproductive season when temperatures were warmer than they have been since 1870, the earliest date for temperature records. Our dispersal dependent mechanistic models of reproductive success were highly accurate and predicted patterns of reproduction success documented in field surveys throughout the historical range in 2015 and 2016. Our mechanistic models of reproductive success not only predicted recruitment dynamics near the range edge but also predicted interior range fragmentation in a number of years between 1870 and 2016. All recruits monitored within the historical range following the 2015 colonization died before 2016 suggesting juvenile survival was likely the primary driver of the historical range retraction. However, if 2016 is indicative of future temperatures mechanisms of range limitation will shift and reproductive failure will lead to further range retraction in the future. Mechanistic models are necessary for accurately predicting the effects of climate change on ranges of species.     

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.     

Species traits and climate velocity explain geographic range shifts in an ocean‐warming hotspot

Species' ranges are shifting globally in response to climate warming, with substantial variability among taxa, even within regions. Relationships between range dynamics and intrinsic species traits may be particularly apparent in the ocean, where temperature more directly shapes species' distributions. Here, we test for a role of species traits and climate velocity in driving range extensions in the ocean‐warming hotspot of southeast Australia. Climate velocity explained some variation in range shifts, however, including species traits more than doubled the variation explained. Swimming ability, omnivory and latitudinal range size all had positive relationships with range extension rate, supporting hypotheses that increased dispersal capacity and ecological generalism promote extensions. We find independent support for the hypothesis that species with narrow latitudinal ranges are limited by factors other than climate. Our findings suggest that small‐ranging species are in double jeopardy, with limited ability to escape warming and greater intrinsic vulnerability to stochastic disturbances.     

Multiple autopolyploidizations and range expansion of Allium przewalskianum Regel. (Alliaceae) in the Qinghai‐Tibetan Plateau

We used the Allium przewalskianum diploid–tetraploid complex on the Qinghai‐Tibetan Plateau (QTP) as a model to examine how this complex responded to the Quaternary climatic oscillations, and whether multiple autopolyploidizations have occurred. We sequenced five chloroplast DNA (cpDNA) fragments (accD‐psaI, trnH‐psbA, trnL‐trnF, trnS‐trnG and rpl16‐intron) in 306 individuals (all of known ploidy level) from 48 populations across the distribution of this species complex. We identified a total of 32 haplotypes—11 in diploids only, 13 in tetraploids only, and 8 found in both cytotypes. This, plus network analyses, indicated that tetraploids have arisen independently from diploids at least eight times. Most populations in the eastern QTP contained multiple haplotypes, but only a single haplotype was found for 17 tetraploid populations on the western QTP, suggesting a recent colonization of the western QTP. We further found that this species complex underwent an earlier range expansion around 5–150 thousand years ago (kya), after the largest glacial period (800–170 kya) in the QTP. In addition, the high frequencies of tetraploids in the QTP suggested that the tetraploid A. przewalskianum cytotype has evolutionary advantages over diploids in colonizing and/or surviving the arid habitats of the QTP.     

Eco‐genetic additivity of diploids in allopolyploid wild wheats

Underpinnings of the distribution of allopolyploid species (hybrids with duplicated genome) along spatial and ecological gradients are elusive. As allopolyploid speciation combines the range of genetic and ecological characteristics of divergent diploids, allopolyploids initially show their additivity and are predicted to evolve differentiated ecological niches to establish in face of their competition. Here, we use four diploid wild wheats that differentially combined into four independent allopolyploid species to test for such additivity and assess the impact of ecological constraints on species ranges. Divergent genetic variation from diploids being fixed in heterozygote allopolyploids supports their genetic additivity. Spatial integration of comparative phylogeography and modelling of climatic niches supports ecological additivity of locally adapted diploid progenitors into allopolyploid species which subsequently colonised wide ranges. Allopolyploids fill suitable range to a larger extent than diploids and conservative evolution following the combination of divergent species appears to support their expansion under environmental changes.