Chloroplast Single Nucleotide Polymorphisms Research Articles

Genomic Screening to Identify Food Trees Potentially Dispersed by Precolonial Indigenous Peoples.

Over millennia, Indigenous peoples have dispersed the propagules of non-crop plants through trade, seasonal migration or attending ceremonies; and potentially increased the geographic range or abundance of many food species around the world. Genomic data can be used to reconstruct these histories. However, it can be difficult to disentangle anthropogenic from non-anthropogenic dispersal in long-lived non-crop species. We developed a genomic workflow that can be used to screen out species that show patterns consistent with faunal dispersal or long-term isolation, and identify species that carry dispersal signals of putative human influence. We used genotyping-by-sequencing (DArTseq) and whole-plastid sequencing (SKIMseq) to identify nuclear and chloroplast Single Nucleotide Polymorphisms in east Australian rainforest trees (4 families, 7 genera, 15 species) with large (>30 mm) or small (<30 mm) edible fruit, either with or without a known history of use by Indigenous peoples. We employed standard population genetic analyses to test for four signals of dispersal using a limited and opportunistically acquired sample scheme. We expected different patterns for species that fall into one of three broadly described dispersal histories: (1) ongoing faunal dispersal, (2) post-megafauna isolation and (3) post-megafauna isolation followed by dispersal of putative human influence. We identified five large-fruited species that displayed strong population structure combined with signals of dispersal. We propose coalescent methods to investigate whether these genomic signals can be attributed to post-megafauna isolation and dispersal by Indigenous peoples.

A Circular Chloroplast Genome of Fagus sylvatica Reveals High Conservation between Two Individuals from Germany and One Individual from Poland and an Alternate Direction of the Small Single-Copy Region

Chloroplasts are difficult to assemble because of the presence of large inverted repeats. At the same time, correct assemblies are important, as chloroplast loci are frequently used for biogeography and population genetics studies. In an attempt to elucidate the orientation of the single-copy regions and to find suitable loci for chloroplast single nucleotide polymorphism (SNP)-based studies, circular chloroplast sequences for the ultra-centenary reference individual of European Beech (Fagus sylvatica), Bhaga, and an additional Polish individual (named Jamy) was obtained based on hybrid assemblies. The chloroplast genome of Bhaga was 158,458 bp, and that of Jamy was 158,462 bp long. Using long-read mapping on the configuration inferred in this study and the one suggested in a previous study, we found an inverted orientation of the small single-copy region. The chloroplast genome of Bhaga and of the individual from Poland both have only two mismatches as well as three and two indels as compared to the previously published genome, respectively. The low divergence suggests low seed dispersal but high pollen dispersal. However, once chloroplast genomes become available from Pleistocene refugia, where a high degree of variation has been reported, they might prove useful for tracing the migration history of Fagus sylvatica in the Holocene.

SNP Markers as a Successful Molecular Tool for Assessing Species Identity and Geographic Origin of Trees in the Economically Important South American Legume Genus Dipteryx.

Dipteryx timber has been heavily exploited in South America since 2000s due to the increasing international demand for hardwood. Developing tools for the genetic identification of Dipteryx species and their geographical origin can help to promote legal trading of timber. A collection of 800 individual trees, belonging to 6 different Dipteryx species, was genotyped based on 171 molecular markers. After the exclusion of markers out of Hardy-Weinberg equilibrium or with no polymorphism or low amplification, 83 nuclear, 29 chloroplast, 13 mitochondrial single nucleotide polymorphisms (SNPs), and 2 chloroplast and 5 mitochondrial INDELS remained. Six genetic groups were identified using Bayesian Structure analyses of the nuclear SNPs, which corresponded to the different Dipteryx species collected in the field. Seventeen highly informative markers were identified as suitable for species identification and obtained self-assignment success rates to species level of 78-96%. An additional set of 15 molecular markers was selected to determine the different genetic clusters found in Dipteryx odorata and Dipteryx ferrea, obtaining self-assignment success rates of 91-100%. The success to assign samples to the correct country of origin using all or only the informative markers improved when using the nearest neighbor approach (69-92%) compared to the Bayesian approach (33-80%). While nuclear and chloroplast SNPs were more suitable for differentiating the different Dipteryx species, mitochondrial SNPs were ideal for determining the genetic clusters of D. odorata and D. ferrea. These 32 selected SNPs will be invaluable genetic tools for the accurate identification of species and country of origin of Dipteryx timber.

Chloroplast and mitochondrial genetic variation of larches at the Siberian tundra-taiga ecotone revealed by de novo assembly.

Larix populations at the tundra-taiga ecotone in northern Siberia are highly under-represented in population genetic studies, possibly due to the remoteness of these regions that can only be accessed at extraordinary expense. The genetic signatures of populations in these boundary regions are therefore largely unknown. We aim to generate organelle reference genomes for the detection of single nucleotide polymorphisms (SNPs) that can be used for paleogenetic studies. We present 19 complete chloroplast genomes and mitochondrial genomic sequences of larches from the southern lowlands of the Taymyr Peninsula (northernmost range of Larix gmelinii (Rupr.) Kuzen.), the lower Omoloy River, and the lower Kolyma River (both in the range of Larix cajanderi Mayr). The genomic data reveal 84 chloroplast SNPs and 213 putatively mitochondrial SNPs. Parsimony-based chloroplast haplotype networks show no spatial structure of individuals from different geographic origins, while the mitochondrial haplotype network shows at least a slight spatial structure with haplotypes from the Omoloy and Kolyma populations being more closely related to each other than to most of the haplotypes from the Taymyr populations. Whole genome alignments with publicly available complete chloroplast genomes of different Larix species show that among official plant barcodes only the rcbL gene contains sufficient polymorphisms, but has to be sequenced completely to distinguish the different provenances. We provide 8 novel mitochondrial SNPs that are putatively diagnostic for the separation of L. gmelinii and L. cajanderi, while 4 chloroplast SNPs have the potential to distinguish the L. gmelinii/L. cajanderi group from other Larix species. Our organelle references can be used for a targeted primer and probe design allowing the generation of short amplicons. This is particularly important with regard to future investigations of, for example, the biogeographic history of Larix by screening ancient sedimentary DNA of Larix.

Development of nuclear and plastid SNP markers for genetic studies of Dipteryx tree species in Amazonia

We developed nuclear and plastid single nucleotide polymorphism (SNP) and insertion/deletion (INDEL) markers for Dipteryx species using a combination of restriction associated DNA sequencing (RADSeq) and low coverage MiSeq genome sequencing. Of the total 315 loci genotyped using a MassARRAY platform, 292 loci were variable and polymorphic among the 73 sampled individuals from French Guiana, Brasil, Peru, and Bolivia. A final set of 56 nuclear SNPs, 26 chloroplast SNPs, 2 chloroplast INDELs, and 32 mitochondrial SNPs identifying significant population structure was developed. This set of loci will be useful for studies on population genetics of Dipteryx species in Amazonia.

Single nucleotide polymorphism analysis in plastomes of eight Catharanthus roseus cultivars

Catharanthus roseus, an important medicinal plant, is known for the production of various pharmaceutical compounds including the anti-tumour drugs, vinblastine, and vincristine. Also, this ornamental plant is widely known for its flowers with different colours. Its varieties are identified on the basis of the morphological characteristics of the flowers, including petals and flower eye colour. Morphological characterization cannot be performed before the flowering stage, leading to a major obstacle for consumers, since most of the sales associated with its medicinal value occur at the vegetative stage. In the present study, we utilized high-throughput, next-generation sequencing to detect chloroplast single nucleotide polymorphism (SNP) that are unique to each variety for molecular characterization. The total genomic DNA of eight C. roseus varieties were sequenced using Illumina HiSeq 2000 platform. The alignment of resulting sequences to chloroplast reference genome showed the presence of specific SNPs for all eight varieties. Also, intravarietal SNPs were found that confirmed the applicability of heteroplasmy theory in the chloroplast genome of this species. Thus, this investigation provides valuable insights into molecular characterization of C. roseus, especially at the vegetative stage.

Comparative chloroplast genomics of series Sakawanum in genus Asarum (Aristolochiaceae) to develop single nucleotide polymorphisms (SNPs) and simple sequence repeat (SSR) markers

ABSTRACTSeries Sakawanum (genus Asarum, Aristolochiaceae) comprises four taxa of forest understory herbaceous plants, which exhibits a geographical cline of calyx lobe length across taxonomic units. To understand the formation process of this series, it is necessary to investigate the evolutionary history based on maternally inherited seed-mediated plastid markers. Using pyrosequencing technique, nearly complete chloroplast genomes of two species (A. minamitanianum and A. costatum) were obtained. Furthermore, nine polymorphic chloroplast single nucleotide polymorphisms (SNPs) and 11 simple sequence repeat (SSR) markers were developed. Most of these markers showed interspecific variations and all markers showed transferability to other Asarum species, while most of markers showed little intra-population variations. These chloroplast genomes and markers can be applied in future studies investigating the contributions of the maternal lineage in shaping the population genetic structure of series Sakawanum and the evolutionary processes underlying their morphological diversification including the characteristic calyx lobe length variation. Moreover, this study showed the applicability of comparative chloroplast genome analysis to develop the chloroplast markers for species group for which it is difficult to obtain polymorphism data using the universal primers.

Development of a set of SNP markers for population genetics studies of Ipe (Handroanthus sp.), a valuable tree genus from Latin America

A combination of restriction associated DNA sequencing (RADSeq) and low coverage MiSeq genome sequencing was used for the development of single nucleotide polymorphisms (SNP) and INDEL (insertion/deletions) genetic markers for Ipe (Handroanthus sp.). Of the 402 putative loci identified, 389 SNPs and INDELs (315 nuclear SPNs, six chloroplast INDELs, 15 chloroplast SNPs, 12 mitochondrial INDELs and 41 mitochondrial SNPs) were successfully genotyped at 93 individuals from Brazil, Bolivia and French Guiana using a MassARRAY® iPLEX™ platform. This set of markers will be invaluable for population genetics, phylogeography and DNA fingerprinting studies

Development of chloroplast single nucleotide polymorphisms (SNPs) as a tool towards interspecies typing ofAnthuriumgermplasm

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Chloroplast genome resources and molecular markers differentiate rubber dandelion species from weedy relatives

BackgroundRubber dandelion (Taraxacum kok-saghyz, TK) is being developed as a domestic source of natural rubber to meet increasing global demand. However, the domestication of TK is complicated by its colocation with two weedy dandelion species, Taraxacum brevicorniculatum (TB) and the common dandelion (Taraxacum officinale, TO). TB is often present as a seed contaminant within TK accessions, while TO is a pandemic weed, which may have the potential to hybridize with TK. To discriminate these species at the molecular level, and facilitate gene flow studies between the potential rubber crop, TK, and its weedy relatives, we generated genomic and marker resources for these three dandelion species.ResultsComplete chloroplast genome sequences of TK (151,338 bp), TO (151,299 bp), and TB (151,282 bp) were obtained using the Illumina GAII and MiSeq platforms. Chloroplast sequences were analyzed and annotated for all the three species. Phylogenetic analysis within Asteraceae showed that TK has a closer genetic distance to TB than to TO and Taraxacum species were most closely related to lettuce (Lactuca sativa). By sequencing multiple genotypes for each species and testing variants using gel-based methods, four chloroplast Single Nucleotide Polymorphism (SNP) variants were found to be fixed between TK and TO in large populations, and between TB and TO. Additionally, Expressed Sequence Tag (EST) resources developed for TO and TK permitted the identification of five nuclear species-specific SNP markers.ConclusionsThe availability of chloroplast genomes of these three dandelion species, as well as chloroplast and nuclear molecular markers, will provide a powerful genetic resource for germplasm differentiation and purification, and the study of potential gene flow among Taraxacum species.

Genetic structure and diversity in Juniperus communis populations in Saxony, Germany

AbstractIn recent years, land use changes led to a rapid decline and fragmentation of J. communis populations in Germany. Population isolation may lead to a restricted gene flow and, further, to negative effects on genetic variation. In this study, genetic diversity and population structure in seven fragmented J. communis populations in Saxony, Germany, were investigated using nuclear microsatellites (nSSR) and chloroplast single nucleotide polymorphism (cpSNP). In all Saxony J. communis populations, a high genetic diversity was determined but no population differentiation could be detected whatever method was applied (Bayesian cluster analysis, F-statistics, AMOVA). The same was true for three J. communis out-group samples originating from Italy, Slovakia and Norway, which also showed high genetic diversity and low genetic differences regarding other J. communis populations. Low genetic differentiation among the J. communis populations ascertained with nuclear and chloroplast markers indicated high levels of gene flow by pollen and also by seeds between the sampled locations. Low genetic differentiation may also provide an indicator of Juniper survival during the last glacial maximum (LGM) in Europe. The results of this study serve as a basis for the implementation of appropriate conservation measures in Saxony.

Tackling intraspecific genetic structure in distribution models better reflects species geographical range.

Genetic diversity provides insight into heterogeneous demographic and adaptive history across organisms’ distribution ranges. For this reason, decomposing single species into genetic units may represent a powerful tool to better understand biogeographical patterns as well as improve predictions of the effects of GCC (global climate change) on biodiversity loss. Using 279 georeferenced Iberian accessions, we used classes of three intraspecific genetic units of the annual plant Arabidopsis thaliana obtained from the genetic analyses of nuclear SNPs (single nucleotide polymorphisms), chloroplast SNPs, and the vernalization requirement for flowering. We used SDM (species distribution models), including climate, vegetation, and soil data, at the whole‐species and genetic‐unit levels. We compared model outputs for present environmental conditions and with a particularly severe GCC scenario. SDM accuracy was high for genetic units with smaller distribution ranges. Kernel density plots identified the environmental variables underpinning potential distribution ranges of genetic units. Combinations of environmental variables accounted for potential distribution ranges of genetic units, which shrank dramatically with GCC at almost all levels. Only two genetic clusters increased their potential distribution ranges with GCC. The application of SDM to intraspecific genetic units provides a detailed picture on the biogeographical patterns of distinct genetic groups based on different genetic criteria. Our approach also allowed us to pinpoint the genetic changes, in terms of genetic background and physiological requirements for flowering, that Iberian A. thaliana may experience with a GCC scenario applying SDM to intraspecific genetic units.

Comparative analysis of single nucleotide polymorphisms in the nuclear, chloroplast, and mitochondrial genomes in identification of phylogenetic association among seven melon (Cucumis melo L.) cultivars.

A variety of melons are cultivated worldwide, and their specific biological properties make them an attractive model for molecular studies. This study aimed to investigate the single nucleotide polymorphisms (SNPs) from the mitochondrial, chloroplast, and nuclear genomes of seven melon accessions (Cucumis melo L.) to identify the phylogenetic relationships among melon cultivars with the Illumina HiSeq 2000 platform and bioinformatical analyses. The data showed that there were a total of 658 mitochondrial SNPs (207–295 in each), while there were 0–60 chloroplast SNPs among these seven melon cultivars, compared to the reference genome. Bioinformatical analysis showed that the mitochondrial tree topology was unable to separate the melon features, whereas the maximum parsimony/neighbor joining (MP/NJ) tree of the chloroplast SNPs could define melon features such as seed length, width, thickness, 100-seed weight, and type. SNPs of the nuclear genome were better than the mitochondrial and chloroplast SNPs in the identification of melon features. The data demonstrated the usefulness of mitochondrial, chloroplast, and nuclear SNPs in identification of phylogenetic associations among these seven melon cultivars.

Whole-chloroplast analysis as an approach for fine-tuning the preservation of a highly charismatic but critically endangered species, Wollemia nobilis (Araucariaceae)

The critically endangered Wollemia nobilis W.G. Jones, K.D. Hill &amp; J.M. Allen is endemic to Wollemi National Park north of Sydney (Australia). All known wild individuals are restricted to four sites in a single canyon system. W. nobilis can reproduce sexually but at all sites individual clumps can be multi-stemmed from a common base. In the first genetic study of this species, no genetic variation was found across multiple genetic marker types representing hundreds of nuclear loci, indicating this species is characterised by very low genetic variation. In this study we searched for variation across the chloroplast using shotgun sequencing, bioinformatic extraction of chloroplast DNA and variant detection. Six chloroplast single nucleotide polymorphisms were detected, producing three chlorotypes. Chlorotype 1 is found in every individual surveyed at Sites 1 and 3, and in individuals from Sites 2 and 4. Chlorotype 2 – the most distinct chlorotype – was found in two individuals from Site 4. Chlorotype 3 consists of a single difference from Chlorotype 1 and may represent a somaclonal mutant. These findings will guide management and translocation of this critically endangered species. This study provides a practical template that is highly informative and easily applicable to other taxa in similar circumstances.

Genetic composition of exotic and native teak (Tectona grandis) in Myanmar as revealed by cpSNP and nrSSR markers

With the rapid fragmentation of tropical forests harboring valuable tree species, conservation of natural genetic resources is an important issue. In Myanmar, teak plantations have been established by Myanmar government since the 1700 s using local Myanmar teak. Commercial plantations have recently been established by the private sector using both exotic and Myanmar teak without consideration of their genetic make-up. If the genetic composition of commercial teak plantations is severely different from that of Myanmar teak, introgression of non-indigenous genes could damage the remaining natural populations. We investigated genetic compositions of commercial plantations using both exotic and Myanmar teak seeds with 10 nuclear simple sequence repeat and three chloroplast single nucleotide polymorphism markers. We then compared the genetic compositions of these populations with those of neighboring native teak forests. The genetic diversity and composition of one exotic plantation using Costa Rican seeds was similar to those of native populations. However, the diversity of the other three exotic plantations was low and their composition was markedly different from those of native populations. Our results suggest that exotic gene flow would cause serious genetic disturbance. Commercial plantations using Myanmar seeds were characterized by relatively high genetic diversity and by many genetic components. These results suggest that these plantations may be established using various seed sources in Myanmar. Given that native teak in Myanmar is geographically structured, native gene pools will be homogenized by gene flow from these commercial plantations. Seed transfer guidelines based on genetic information should be considered in future.

Where did all the trees come from? A novel multispecies approach reveals the impacts of biogeographical history and functional diversity on rain forest assembly

AbstractAimWe take advantage of next generation sequencing‐based technology to assess how landscape‐level dynamics, biogeographical history and functional factors shape the distribution of genetic diversity in rain forest trees. To achieve this, we explore chloroplast genomic diversity and divergence patterns across multiple, co‐distributed species from three major centres of rain forest diversity.LocationSubtropical rain forests in south‐eastern Australia: Nightcap–Border Ranges, Dorrigo and Washpool.MethodsWe assembled chloroplast genomic data from whole‐genome shotgun libraries for 71 species collected across three major centres of rain forest diversity. Chloroplast single nucleotide polymorphisms were used to measure genetic variation within and between multiple populations, species and locations, and we used this information to identify patterns related to landscape‐level processes, biogeographical origins and functional characteristics.ResultsWe identified Nightcap–Border Ranges and Dorrigo as containing multiple refugia and Washpool as primarily a recolonized area. We found that rapidly expanding lineages of Indo‐Malesian origin exhibit significantly lower levels of genetic diversity than Gondwanan lineages with longer local histories. Functional traits related to persistence and dispersal were the most important in regulating the distribution of genetic diversity.Main conclusionsThe distribution and assembly of species reflect interactions and competition between different floristic elements at different stages of continental occupation. Additionally, given the multiple evolutionary origins and histories of the Australian rain forest flora, it is important to avoid treating rain forest communities as single management units.

Current Genetic Structure of Teak (Tectona Grandis) in Myanmar Based on Newly Developed Chloroplast Single Nucleotide Polymorphism and Nuclear Simple Sequence Repeat Markers

Teak ( Tectona grandis), which is among the most valuable tropical timber species, is under pressure from rapid deforestation and habitat fragmentation. Limited genetic information is available for Myanmar teak, which comes from the largest natural teak-bearing forest area in the world. To determine the phylogeographic patterns of Myanmar teak, we evaluated three newly developed chloroplast single nucleotide polymorphism (cpSNP) and 10 nuclear simple sequence repeat (nrSSR) markers in 480 individuals representing 20 natural populations. The cpSNP markers detected four haplotypes, each differing by a single mutation. The GST value was lower than the NST value and did not reveal a phylogeographic structure of Myanmar teak. Nuclear microsatellite analysis revealed high genetic diversity with the mean expected heterozygosity (0.652). The same level of genetic differentiation (4%) was observed for both cpSNP and nrSSR markers in different groups. Conservation of the HMB, TDG, KTA, and POL populations should receive highest priority because these contribute most to the total genetic diversity. The genetic boundaries of teak observed from combining the results of cpSNP and nrSSR marker barriers suggested four potential zones in the teak seed transfer guidelines of Myanmar. In light of our findings, we discussed appropriate gene conservation strategies and proposed seed zones to safeguard the current genetic resources of Myanmar teak.

Bioclimatic, ecological, and phenotypic intermediacy and high genetic admixture in a natural hybrid of octoploid strawberries

Hybrid zones provide "natural laboratories" for understanding the processes of selection, reinforcement, and speciation. We sought to gain insight into the degree of introgression and the extent of ecological-phenotypic intermediacy in the natural hybrid strawberry, Fragaria × ananassa subsp. cuneifolia. • We used whole-plastome sequencing to identify parental species-specific (Fragaria chiloensis and F. virginiana) chloroplast single-nucleotide polymorphisms and combined the use of these with nuclear microsatellite markers to genetically characterize the hybrid zone. We assessed the potential role of selection in the observed geographic patterns by bioclimatically characterizing the niche of the hybrid populations and phenotypically characterizing hybrid individuals of known genomic constitution. • Significant admixture and little overall maternal bias in chloroplast or nuclear genomes suggest a high degree of interfertility among the parental and hybrid species and point to a long history of backcrossing and genetic mixing in the hybrid zone. Even though hybrids were phenotypically intermediate to the parental species, there was a discernible fingerprint of the parental genotype within hybrid individuals. Thus, although the pattern of introgression observed suggests geographic limitations to gene flow, it may be reinforced by selection for specific parental traits in the bioclimatically intermediate habitat occupied by the hybrid. • This work uncovered the genetic complexity underlying the hybrid zone of the wild relatives of the cultivated strawberry. It lays the foundation for experimental dissection of the causes of genomic introgression and nuclear-cytoplasmic disassociation, and for understanding other parts of Fragaria evolutionary history.

Differentiation of Populus species using chloroplast single nucleotide polymorphism (SNP) markers – essential for comprehensible and reliable poplar breeding

Within the genus Populus several species belonging to different sections are cross-compatible. Hence, high numbers of interspecies hybrids occur naturally and, additionally, have been artificially produced in huge breeding programmes during the last 100 years. Therefore, determination of a single poplar species, used for the production of 'multi-species hybrids' is often difficult, and represents a great challenge for the use of molecular markers in species identification. Within this study, over 20 chloroplast regions, both intergenic spacers and coding regions, have been tested for their ability to differentiate different poplar species using 23 already published barcoding primer combinations and 17 newly designed primer combinations. About half of the published barcoding primers yielded amplification products, whereas the new primers designed on the basis of the total sequenced cpDNA genome of Populus trichocarpa Torr. & Gray yielded much higher amplification success. Intergenic spacers were found to be more variable than coding regions within the genus Populus. The highest discrimination power of Populus species was found in the combination of two intergenic spacers (trnG-psbK, psbK-psbl) and the coding region rpoC. In barcoding projects, the coding regions matK and rbcL are often recommended, but within the genus Populus they only show moderate variability and are not efficient in species discrimination.

Unidirectional hybridization at a species’ range boundary: implications for habitat tracking

AbstractAim Introgressive hybridization between a locally rare species and a more abundant congener can drive population extinction via genetic assimilation, or the replacement of the rare species gene pool with that of the common species. To date, however, few studies have assessed the effects of such processes at the limits of species’ distribution ranges. In this study, we have examined the potential for hybridization between range‐edge populations of the wintergreenPyrola minorand sympatric populations ofPyrola grandiflora.Location Qeqertarsuaq, Greenland and Churchill, Manitoba, Canada.Methods Genetic analysis of samples from Greenland and Canada was carried out using a combination of nuclear and chloroplast single nucleotide polymorphisms (SNPs).Results Analysis of nuclear SNPs confirmed hybridization in populations of morphologically intermediate individuals, as well as revealing the existence of cryptic hybrids in ostensibly morphologically pureP. minorpopulations. Analysis of chloroplast SNPs revealed that this hybridization is unidirectional and suggests that hybrids originate via pollen swamping ofP. minorby the more commonP. grandiflora.Main conclusions Extensive unidirectional hybridization may lead to the extinction of peripheral populations ofP. minorwhere the two species grow sympatrically. Extinction could occur as a result of genetic assimilation where F1s are fertile, or via the removal of unidirectionally pollinated sterile F1s, or by a combination of these processes. This could compromise the ability of species to respond to climate change via habitat tracking, although the final outcome of these processes may ultimately depend on the rate of global climate change and its effect on the species’ distributions.