History of Insect Collection and a Review of Insect Diversity in Sri Lanka
Philos Trans R Soc Lond B Biol Sci. 2019 January seven; 374(1763): 20170405.
Using insect natural history collections to study global change impacts: challenges and opportunities
Heather Thou. Kharouba
1Department of Biology, University of Ottawa, Ottawa, Ontario, Canada, K1N 9B4
Jayme M. M. Lewthwaite
twoDepartment of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, Canada, V5A 1S6
Rob Guralnick
iiiDepartment of Natural History and the Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, U.s.a.
Jeremy T. Kerr
oneDepartment of Biology, University of Ottawa, Ottawa, Ontario, Canada, K1N 9B4
Marker Vellend
4Département de Biologie, Université de Sherbrooke, Sherbrooke, Quebec, Canada, J1 K 2R1
Abstract
Over the by two decades, natural history collections (NHCs) have played an increasingly prominent part in global change research, but they have still greater potential, especially for the most diverse grouping of animals on Earth: insects. Here, nosotros review the part of NHCs in advancing our agreement of the ecological and evolutionary responses of insects to recent global changes. Insect NHCs take helped document changes in insects' geographical distributions, phenology, phenotypic and genotypic traits over time periods up to a century. Recent work demonstrates the enormous potential of NHCs data for examining insect responses at multiple temporal, spatial and phylogenetic scales. Moving forwards, insect NHCs offer unique opportunities to examine the morphological, chemical and genomic information in each specimen, thus advancing our understanding of the processes underlying species' ecological and evolutionary responses to rapid, widespread global changes.
This article is office of the theme consequence 'Biological collections for understanding biodiversity in the anthropocene'.
Keywords: specimens, museum, range shifts, climate change, seasonal timing
1. Introduction
The unprecedented velocity of modern climatic change, and its interaction with other global alter drivers (east.thousand. land-utilise alter, species introductions), has made it hard to forecast the future construction and office of ecological communities. Recent evidence suggests widespread variation within and beyond taxonomic groups in species' responses to global change (e.g. [1,two]). Moreover, attempts to use biological characteristics like ecological or life-history traits to explain some of this variation have had varying degrees of success (east.thou. [3,iv]). Agreement the causes and consequences of this variation remains critical in order to anticipate the ecological and evolutionary impacts of global alter.
For centuries, natural history collections (NHCs) take been disquisitional for basic biological research (e.g. taxonomy, systematics [5]). Over the past 2 decades, these collections accept played an increasingly vital role in detecting plant [six] and fauna [5] species' ecological and evolutionary responses to global change. Even so, use of NHCs in insect global change studies are still rare and most efforts are oft restricted to a few species, minor geographical areas and brusk timeframes [7,eight]. Past providing information on the place and time of drove, specimens can be used to generate spatio-temporal data on the geographical distribution, phenology and other phenotypic traits of organisms. Billions of specimens take been collected all around the world over the past century [5], such that collections tin can provide the long-term and broad spatial extents needed to decide the influence of multi-scale ecology change on diverse taxa.
Insects are the most diverse taxon on Earth, but they are vastly under-represented in global change inquiry, especially relative to their diversity [9]. The most charismatic insect groups, like butterflies, are abundant in NHCs, providing a remarkable and underused resources, and a wealth of opportunities for global change research [nine]. Insects play integral roles in ecological communities and ecosystems equally herbivores, predators, pollinators and prey. As ectotherms, insects are highly sensitive to temperature and are oft used as indicators of environmental alter for other organisms [10,11]. Irresolute climates can straight affect insect species in several ways: including physiologically, developmentally, behaviourally or indirectly through interspecific interactions (east.g. chastened through changes to a host plant) [12]. Previous reviews have focused on the valuable part of institute collections (herbaria) in global modify research (due east.g. [thirteen,fourteen]), but few, if whatsoever, take synthesized the overall contribution of insect collections.
The aim of this review is to provide an overview of the challenges and opportunities associated with using insect collections to detect and sympathise the influences of the master drivers of global change—especially climate and land-apply changes—over the past century. We focus our review on the all-time-studied ecological and evolutionary responses: geographical distributions and phenology (i.eastward. the timing of recurring life-history events), too every bit other primal phenotypic and genotypic characteristics such equally body size and melanism. Nosotros focus on responses inside individual species rather than on emergent properties of biological communities.
(a) Nature of the data
Through curated collections of individual specimens, NHCs provide straight evidence of: (i) a species occurring at a detail location at a particular point in fourth dimension; (ii) the identification of that species' life stage (e.g. adult); and (iii) its morphological traits (e.m. wing size [fifteen]). Depending on the collection effort for a given species, specimens housed in NHCs are probable to have been collected from many sites across its geographical range and from unlike time periods; however, there is ofttimes high variation in sampling intensity for both dimensions. Because these collections necessarily consist of presence-only data, and specimen collection often reflects opportunistic sampling rather than long-term monitoring of particular sites, NHCs mostly provide limited means to depict inferences about a particular species in a given location or even presence at a item site, except for very well-collected species and locations. Inconsistent or incomplete sampling is a general problem in detecting species' responses to global change that plagues many long-term datasets [16]. In a meta-analysis with other sources of distribution data (including species atlases and citizen scientist observations), museum information were found to be the nigh cosmopolitan [17]. While we recognize that NHCs are often used in combination with other information sources (e.g. using field-based occurrence information to assess a species' current geographical range), hither we focus on global change enquiry but fabricated possible by insect NHCs (east.thousand. estimating historical range shifts).
Following Meyer et al. [xviii], we distinguish three terms related to taxonomic, geographical and temporal data associated with NHCs: coverage, uncertainty and bias. Coverage is closely related to the quantity of records whereas incertitude is associated with the quality of data on each specimen. Bias arises when observations represent not-random samples with respect to particular quantities of interest. For example, geographical coverage of drove records may be biased towards areas close to towns with universities [19], simply this does not necessarily constitute bias with respect to the environmental conditions across a given species range (eastward.chiliad. if academy towns are randomly distributed with respect to the climate within the species' range).
In the next section, nosotros review the literature on the four fundamental applications of NHCs—geographical changes, phenological, other phenotypic (e.yard. morphological) responses and genetic responses—aimed at understanding insect responses to global alter. For each application, nosotros discuss fundamental challenges and opportunities for future inquiry.
two. Application 1: geographical changes
Over the past century, there take been ii major causes of changes in species' geographical distributions: (i) climate and/or land-utilize change-driven redistributions within continents (e.g. [1,twenty]); and (two) intentional or non-intentional introductions to new continents or new areas within continents and their subsequent spread. Detection and attribution of causes of species' geographical range shifts require the measurements of species' ranges from multiple fourth dimension periods [21,22]. NHCs have been particularly valuable in documenting 'historical' ranges, thus providing crucial baselines for detecting ongoing and widespread range shifts in many groups, including butterflies [23], spiders [24], dragonflies [25] and grasshoppers [26].
Understanding past species' responses to global alter or introduction to novel environments informs predictions of the impacts of future ecology changes and, for some species, prospects for conservation. For example, NHCs were used to reveal larger range losses and slower distribution shifts in threatened versus non-threatened butterflies in Finland [27]. They were as well used to show that the period of greatest range contractions and local extirpations in many bumblebee species in Illinois over the past century coincided with large-scale agricultural intensification during the middle of the century [28]. In both Europe and North America, NHCs were instrumental in demonstrating the failure of many bee and butterfly geographical ranges to track shifting climates ('climatic debts' [29–31]), and particularly acute range losses in the warmest (southern) areas [30,31]. NHCs immune estimates of climatic debts over much longer fourth dimension scales than recent constitute-focused studies [32,33]. When directly compared, flying insects show smaller climatic debts than more mobile groups like birds [29], probably because they have shorter life cycles and are ectothermic.
To quantify climatic debts, NHCs provide the critical historical observations for parametrizing climate-based niche models (effigy 1), which are projected (from past to present) and compared to current distributions [34]. A prerequisite for robust forecasting is the ability of models to predict changes that have already occurred [35] and these climate-based niche models accept shown some success in predicting northern range shifts of Canadian butterflies over the past few decades [23,34].
A demonstration of the role of NHCs in modelling species distributions using the Atlantis fritillary butterfly (Speyeria atlantis) equally a case written report. (a–d) Environmental niche models (ENMs) constructed using ii sources of data: (a,b) NHCs and (c,d) not-NHCs. Models were calibrated on 1900–1975 distribution points (a,c) using an ensemble approach. The cross-validated, consensus ENM was then projected using contemporary (1985–2010) climatic conditions to model potential distributions (b,d). Observed distribution data for each respective time menstruation is overlaid (black dots). Run into [34] for a complete description of the modelling methods. Goodness of fit for each ENM was measured using area under the bend (AUC) and the truthful skill statistic (TSS). Too shown is a chief component (PC) analysis of the climate space occupied by S. atlantis from (e) 1900 to 1975 and (f) 1985 to 2010, where light-green points are NHCs and orangish are non-NHCs (95% confidence intervals (CIs) are indicated by the ellipses). Occurrence data from NHCs are from the Smithsonian Institute's National Museum and Global Biodiversity Information Facility (GBIF), and the occurrence data from non-NHCs included: eButterfly, the Toronto Entomological Association and records from GBIF non labelled every bit a museum collection. (Online version in colour.)
NHCs take been used less frequently to study species invasions than to study native species' range shifts. They can provide invaluable historical occurrence data [17] that help distinguish historically unprecedented introduction and range expansion events from periodic recolonizations of a given geographical area [36]. A common use for NHCs is in the quantification of a species' native range [19], from which niche models tin can exist constructed and and then used to predict potentially suitable areas in the introduced range—an approach that has been practical to a couple of Asian beetle species in North America [37]. NHCs have as well been used to determine the timing of initial establishment of exotic ants on islands [38] and the harlequin ladybird beetle (Harmonia axyridis) in South Africa [39], also equally the rates of range expansion of exotic ant species [40]. Assembling observations across entire biological communities from NHCs have been used to measure the impacts of invasive ant species on community structure [38].
NHCs can be used to understand conditions enabling successful invasions [40,41]. For example, Ward et al. [40] used NHCs to make up one's mind that new occurrence records of the Argentine ant in New Zealand were likewise far from known populations to be explained by natural dispersal and ended that human-mediated dispersal was the chief commuter of invasive spread. For a globally widespread invasive ant species (Linepithema humile), Roura-Pascual [41] used NHCs to show that climatic suitability and extent of human-modified habitats best predicted invasive spread. Despite the well-known link between human presence and the distribution of invasive species, relatively few studies have specifically tested man influence every bit a driver.
(a) Challenges
Detecting and explaining geographical range shifts amid insects or other taxa using NHCs is challenging for several reasons. First, specimen collections typically practise not provide information nigh species' absences [42]. 2nd, geographical coverage of records is typically biased towards accessible, populated or economically prosperous regions. Inaccessibility has limited Arctic insect collection [43] relative to other areas, and exploration of insect diversity in persisting wilderness areas remains severely limited [42]. Although many NHC databases are global in their focus (such every bit the Global Biodiversity Information Facility), they are notably data-deficient in some of the earth's biodiversity hotspots [44] and data concentration is skewed towards northern temperate latitudes [45]. For some applications (due east.g. niche modelling), geographical gaps in sampling matter but to the extent that gaps are biased towards particular combinations of environmental weather condition [19] (figure 1), as was found to exist the case for most of the dung beetle species' modelled in the Madrid region of Spain [46]. Geographical doubt, typically more problematic in historical records, too further reduces our power to detect range shifts.
Collection gaps near species' range margins, where populations may already be sparse [47] and imperceptible [48], create acute challenges for determining whether a 'new' observation in a given surface area represents range expansion or simply a failure to observe historical presence. In the context of climate warming in the northern hemisphere, a lack of northern records either early on or late in the information tape could lead, respectively, to commission errors (predicting range expansion when information technology did not occur) or omission errors (predicting no range expansion when it did occur).
Thin temporal coverage (both within and across years) and biases likewise present challenges. Insect species, even when common and/or highly mobile, can be missed in well-nerveless areas if they have brusque-lived adult life stages and specimens are collected over brief time periods [42]. There is a little quantification of temporal bias in insect collections only some prove for bumblebees in N America suggests geographical variation in sampling intensity changes over the past 120 years (effigy ii). Comparatively, at that place have been increases in collections over time for Canadian butterflies [49]. These patterns contrast with some herbaria where the frequency of collections has declined in recent decades every bit field biologists shifted from taxonomic to ecological studies [fifty,51].
Differences in sampling intensity for bumblebees in eastern Northward America between 1900–1975 and 1976–2010. Blocked out areas of dark greenish show increasing sampling intensity, while red colours point declining sampling intensity betwixt these time periods. Areas of light grayness were sampled in the get-go time period simply not in the second, and areas in dark grey were sampled in the second time menstruum and not earlier for this grouping of species. The background is MODIS land cover data for North America (250 1000 resolution) for 2005. The inset histogram shows variation in sampling intensity with respect to latitude betwixt the time periods, with red showing sampling in the earlier time period and calorie-free showing sampling by latitude in the later time period. See [31] for a complete list of data sources and methods. (Online version in colour.)
More broadly, there is a scarcity of insect range-shift studies in Asia, Africa and S America (although this is beginning to change; e.g. [52]). We might also expect—as is the instance for plants [50]—less frequent sampling of non-native species, even in countries with strong collecting traditions. Recent digitization initiatives such as the Darwin Initiative and the Advancing Digitization of Biodiversity Collections programme in the Us, have begun profitable in these efforts [35].
(b) Opportunities
Contempo advances in occupancy modelling aim to increase the robustness of estimates of range changes given uncertainties in NHC data for insects and other taxa [22]. Addressing sampling gaps is vital in global modify applications of NHC data and new techniques in Bayesian and maximum-likelihood models [53] offer great improvements over algorithms that do not account for sampling biases. For detecting range shifts, 1 cardinal advance is the probability of false absence tests (Pfa), which incorporate the number of surveys across a set of unoccupied sites to calculate the likelihood of a historic absence [22]. This arroyo provides a confidence judge for observations of absence, helping to distinguish bodily range shifts from credible range shifts owing to data limitations (i.eastward. imitation absences in the historical information). Another advance is the use of a maximum probability approach where a species' environmental optimum is determined based on the maximum probability of occupancy across an environmental gradient [54]. Whatever recently documented range shift (and the ecology conditions within the colonization zone) is compared to the historical optimal range to gauge whether it is more than probable to be a true shift in distribution or a temporary fluctuation in a range limit [53]: newly occupied sites that are closer to a species' optimal atmospheric condition are considered more than probable shifts rather than fluctuations. A major caveat of both of the above occupancy models is that they require repeated surveys at the same locations, which are rare in most NHCs. With further improvements in occupancy models, nosotros are optimistic that they can provide useful predictions of futurity range shifts.
Relative to their use in documenting range shifts of native species, NHCs have been vastly underused in recording the spread of introduced insects. Moreover, insects have received far less attending compared with other taxa, such equally plants, vertebrates and aquatic organisms [vi,55], yet their geographical distributions are predicted to expand in the time to come to a greater degree than other groups like plants and birds [56]. For studies of introduced species, methods are being adult and practical in other taxa to business relationship for biases such every bit the nether-sampling of non-native species, including curves that compare the cumulative area occupied by native versus introduced species [50]. In poorly sampled areas, the ranges of native species may increase through time simply as a function of improved spatial sampling and coverage; quantifying such credible range expansion provides a baseline 'null' rate confronting which to compare introduced species [50]. While this approach has been applied to herbarium specimens of several invasive institute species [50], it has not notwithstanding been applied to insects.
Insect NHCs tin can also provide information about changes in the geographical distribution of other taxonomic groups. Insect specimens could be examined for the presence of parasitoids, parasites, pathogens or fifty-fifty pollen [57]. For instance, the composition of pollen loads on the specimens of bumblebees in northwestern Europe was used to show distribution changes in flowering plant taxa over the past century, including the spread of an invasive plant species [58].
3. Application two: phenological responses
Despite the potential of NHCs to provide phenological data over long timeframes [35], they accept only recently been used as a tool to measure phenological shifts owing to climate change, a ordinarily documented response. Moreover, very few studies have focused on insects. Insect NHCs most frequently consist of specimens of adults. Therefore, NHCs tin can be used to estimate the timing (phenology) of adult activity. NHCs have been shown to provide estimates of phenology comparable to those generated using field observations, despite possible biases inherent in both types of data [17,51]. For case, the average drove date of bee collections was constitute to exist a valid proxy for peak adult activity in bees estimated from field observations [59]. Comparisons to the 10th percentile for mean first appearance date were also found to be accurate [51].
Thus far, NHCs accept been used to show that over the by century in Northward America, the UK and Europe, Lepidoptera (mostly butterflies) and bees have shifted the timing of adult activeness earlier in the year and increased the number of generations per year [49,59–64] over the past century. NHCs take besides helped to shed light on variation in temperature sensitivity of phenology (days °C−1) inside [49,51] and across taxonomic groups like bees [59,63] or collywobbles [64,65] and their host plants, or between different types of pollinators [62]. Estimates of phenological sensitivity to temperature using NHCs announced to be comparable to estimates derived from other methodological approaches ([62]; just see [59]). Understanding interspecific variation in temperature sensitivity is a primal challenge for future research as species with unlike temperature sensitivities are likely to show different responses to global changes.
(a) Challenges
While some studies using NHCs have demonstrated insect phenological shifts over time, other studies did not discover temporal trends [49,59–64]. The detection of directional phenological trends over time has been shown to depend on the ecological or life-history strategy of the species (e.one thousand. generation length [49,62]), the type of data (eastward.g. atlas versus incidental sampling [62]) and the timeframe of study [65] (figure 3). This is unsurprising given that long-term phenological trends are hands obscured by interannual variation [66]. This is exacerbated when there is low and/or uneven temporal coverage (within and across years) for species in NHCs, or in the presence of large interannual variation in temperature across locations [65]. Together, these issues can lead to increased incertitude around estimates of phenological shifts (figure 3). Indeed, studies using NHCs are less probable to observe phenological trends than studies of the same species using direct and systematic observations (due east.g. [51] versus [67]). Kharouba et al. [49] suggest that at least, at broad scales, the difference is unlikely to exist attributable to temporal sampling biases of collywobbles (due east.m. systematically surveying earlier in warmer years). However, the likelihood of these biases remains to exist formally tested.
The relationship between uncertainty effectually estimates of butterfly species' phenological shifts (days/year) over the by century across Canada and the length of time frame (years) for each species (n = 196). Uncertainty was measured as the length of the 95% CI for each guess of phenological shift (days/year). The distribution of number of records across species is shown. The line of best fit with the 95% CI (y = 0.ix–0.02x + 0.0008x 2) is also shown. Data were taken from [49]. (Online version in colour.)
NHCs have shown more potential for quantifying interspecific variation in the sensitivity of adult flying timing to temperature. Even so, adult flight fourth dimension may not be representative of other life stages: recent show shows that there is variation across ontogenic stages in temperature sensitivity [68,69] and the metric of the temperature of greatest relative importance [seventy]. Therefore, organisms with complex life cycles, where dissimilar environments are experienced during different life stages, are likely to have differing responses of each life stage [68].
Finally, given the complexity inherent to phenological records assembled over long timeframes (due east.g. temporal autocorrelation, not-stationarity), there are statistical challenges when applying NHCs to detect and empathize phenological responses of insects and other taxa to climate change [71,72]. Even so, these issues are rarely accounted for in studies using NHCs, potentially affecting the robustness of their conclusions. Recent advances in statistical techniques and approaches aim to deal with these complexities more rigorously. For example, MacGillivray [73] established the existence of nonlinear trends in peak flowering using herbarium records by applying generalized condiment models for location, scale and shape. Bayesian approaches can more than comprehensively business relationship for uncertainty [71] and the contempo developments of more accessible packages (e.g. Stan (www.mc-stan.org)) in open-source statistical computing platforms (e.g. R (www.r-projection.org)) volition hopefully increase the application of these methods to phenology studies using NHCs.
(b) Opportunities
An as-still underexplored opportunity using NHCs is to apply the sex associated with specimens to exam for differential responses of male and female insects to climatic change. Distinguishing responses betwixt sexes could assist understand the impacts of climate change on the success of mating processes, effectiveness of pollination and refine estimates of species-level phenological sensitivity to temperature [59]. For example, studies using NHCs have found that female butterflies are flight progressively earlier in recent decades than males [64] and female bees are more responsive to temperature than males [59].
NHCs may as well provide a critical but so far underused resource for examining the possibility of shifts in the timing of species interactions over longer time scales and with more than species than local field studies. A recent exemplary study past Robbirt et al. [59] used NHCs for plants and insects (roofing greater than 100 years), along with field observations, and showed that a pollinator and its host showed differential phenological responses to climate change, which is likely to atomic number 82 to temporal mismatches nether future climate scenarios. The rapidly expanding digitization of NHCs could greatly expand the potential for addressing phenological mismatch questions.
iv. Application 3: responses in phenotypic traits
Insect NHCs provide not only spatial and temporal occurrence data, but whole preserved organisms, and therefore the possibility of examining phenotypic responses to global change. Particularly notable are studies of trunk size responses to global changes [70,74–77]. These studies are among the commencement to explore global alter-driven body size changes in insects, a group whose body size changes were previously not well studied [78]. For case, stream-dwelling beetles in the southern United states [64] and the butterfly Melitaea cinxia in Sweden [79] have increased in torso size in recent decades owing to land-employ [79] and climate changes [64]. Conversely, predatory bugs (Orius; Heteroptera: Anthocoridae) in Israel [76] and a population of wild honeybees (Apis mellifera) in the Us [80] have shown no change [76] or a pass up in body size over the past few decades [76]. Based on results from studies on beetles in State of israel [76] and British Columbia, Canada [77], some of the interspecific variations in temporal changes in body size can exist deemed for past the hateful trunk size of the species, with larger bodied beetles decreasing in size over time the most [77]. Every bit Bartomeus et al. [81] showed with almost 50 000 bee specimens, a larger body size, as well as a limited phenological latitude (i.due east. number of days of adult activity per yr), can likewise correlate with a decreased abundance over time in the face of climate change. Using NHCs allowed these last few studies to move across the documentation of localized furnishings on body size and to define broad-scale patterns in trunk size changes in response to climate change.
NHCs have as well been used to report phenotypic traits—other than body size—underlying evolutionary responses of insects to global changes. For case, Carroll et al. [82] showed that the mouthparts of the Australian soapberry bug (Leptocoris tagalicus), measured on NHC specimens, have increased significantly in size to take reward of larger fruits from an invasive Neotropical airship vine (Cardiospermum grandiflorum). Traits that affect thermoregulatory chapters, such as wing melanism and torso size, are expected to respond to climate warming. Notwithstanding, MacLean et al. [83] plant results counter to expectations: fly melanism and body size in the sulfur butterfly (Colias meadii) was found to increase with warming temperatures over time, thus challenging models of evolutionary response to global changes.
(a) Challenges
Similar to the other applications, uneven sampling efforts can limit the ability to detect trait changes in studies based on insect NHCs. Data for most insect taxa are too sparse to measure shifts in particular species' traits through time or across environmental gradients. This is particularly problematic for more than integrative studies that aim to consider multiple responses simultaneously and are thus data-hungry. Where such records take non been collected in the past, there is no solution to this challenge. However, the digitization of collections, with specimen imaging and rapid expansions of databases containing curated specimen information in standardized formats, promises to betrayal particularly useful historical collections for written report and for potential targeted resurveys (east.g. [84]).
(b) Opportunities
Integrative studies that fully use NHCs, now enabled via digitization, are notwithstanding emerging. I of the nearly exciting research avenues volition require more than just digital products: physical specimens offer untapped potential for isotopic studies [85]. Ratios of stable carbon and nitrogen isotopes in specimen tissues provide a tape of diet and habitat change through time and allowed English language et al. [85] to infer a pass up in the contribution of insects to insectivorous bird diets over a 125-year period. More mutual applications of cutting edge imaging techniques such as micro-computed tomography scanning, hope to provide dense internal and external morphological information [86] coupled with three-dimensional morphometric approaches. For example, taxonomically of import characters, such as genitalia in male Lepidoptera, can be distinguished using pinned specimens [86]. Application of these approaches using insect NHCs is in its infancy.
5. Awarding four: responses in genotypic traits
Specimens from NHCs are increasingly existence used for the genetic and genomic information they harbour to aid shed light on the evolutionary component of species responses to global change. With the appearance of next-generation sequencing and optimization of Dna extraction techniques, it has get much easier to successfully extract and sequence Dna from museum specimens [87], including insects. Sequencing studies across a species' range oftentimes look for signals of adaptation to spatial environmental variation [88] and the same conceptual approach could exist applied temporally. By providing historical samples earlier episodes of environmental change, NHCs can provide a means of inferring demographic changes (due east.g. population declines or expansions) over time [89]. For example, Mikheyev et al. [fourscore] conducted whole genome sequencing on individuals from NHCs and current populations. Their results suggest that genetic diverseness may accept buffered populations of wild honeybees (Ap. mellifera) through bottlenecks acquired by introduced Varroa mite parasites. Similarly, historical NHCs for four British bumblebee species that were introduced in New Zealand were compared to mod populations to written report the genetic impact of 100-yr old population bottlenecks and novel environments [90]. NHCs of the garden tiger moth (Arctia caja) in the UK were used to reveal a loss of genetic diversity, equally well equally meaning changes in fly size and shape, post-obit a widespread population crash in the 1980s [91].
Molecular genetic and genomic approaches are also yielding insights into insect invasions. NHCs offer unique opportunities to examine the genetic variation of populations during the multiple stages of invasions over long time scales [57]. Recently, Cridland et al. [92] used museum specimens of the introduced honeybee (Ap. mellifera) to analyse the impact of demography and selection on introduced populations during the by century. They discovered hundreds of candidate genes underlying recent adaptations, including potential resistance to parasitic mites in their invaded range. Herbaria can also provide information about historic insect distributions. Using Dna from larvae of a leaf-mining moth (Cameraria ohridella) pressed inside leaves of herbarium samples collected as early as 1879, Lees et al. [93] revised the date of introduction of this herbivorous species to Europe by more than a century and uncovered previously unknown mitochondrial haplotypes and locally undocumented alleles. The authors also documented genetic homogenization beyond the species' range post-obit the invasion, which led to questions virtually how allele frequencies have changed, and whether these are associated with any genes that enable invasion success [93].
(a) Challenges
Using NHCs to explore evolutionary responses to global changes face some unique challenges that bear on inferences fabricated about insects and other taxa. First, given the low sample size and inconsistent spatio-temporal sampling typically associated with insect NHCs, specimens are sometimes pooled to obtain a useful sample size only this can reduce overall heterozygosity [90]. Second, there remain few reference genomes for insects (relative to their diversity), which can complicate genome assembly and the assessment of cistron part. Third, in addition to the sampling biases mentioned in earlier sections, sure morphotypes of a species may be more likely to be captured owing to visibility (e.g. more than colourful) or ease of detection (eastward.g. larger), resulting in biased samples of genetic variants in a given population [89,94]. Lastly, erstwhile specimens may accumulate more than DNA damage, which tin produce biases in genome mapping [80]. Nevertheless, some potential biases, for case in allele frequencies, can exist tested against theoretical expectations from population genetics to help guide quality control [lxxx].
(b) Opportunities
To engagement, there have been few studies applying genetic and genomic approaches to insect NHCs, only there is great potential [89]. For example, in other taxa, researchers have combined NHCs with modern data to (i) improve our agreement of the genetic consequences of range dynamics (e.thousand. in chipmunks [95]); and (ii) predict future vulnerability of populations to climate change based on relationships between allele frequencies and climate variation (e.g. in a migratory bird [96]). Genetic data could besides aid identify potential source populations that are pre-adapted to the environmental conditions in target sites for assisted colonization [97]. With the chop-chop failing costs of molecular analyses and the availability of new approaches that are well-suited for the type of Dna that is mutual in historical specimens (i.e. small-scale amount, fragmented), nosotros anticipate a wave of new studies based on DNA extracted from NHCs to accost a wide range of bug involving rapid development, demographic changes or the consequences of invasive spread.
half dozen. Terminal remarks
NHCs accept made important and unique contributions to our understanding of how insects are responding to global change. In many of the studies we reviewed, NHCs provided the simply means of achieving the necessary temporal depth to examine long-term modify in distributions, phenology, morphological traits or genetic variation. While historical sampling is one of the most unique benefits of NHCs, it is likewise one of the biggest challenges: historical information are often accompanied past uneven coverage and sampling biases in space and time. Even so, recent work demonstrates the enormous potential of NHCs for examining insect responses at multiple temporal, spatial and phylogenetic scales.
We have outlined several inquiry avenues to raise the role and bear upon of NHCs in understanding and predicting the ecological and evolutionary consequences of climate change for insects. Here we can highlight the overarching event of more than carefully defining baselines that predate rapid contempo warming (e.one thousand. earlier the early 1980s in some regions [21]). Defining advisable baselines tin can put shorter-term trends (i.eastward. 5–30 years) into context against longer-term trends (i.e. past century) and natural fluctuations [16,70]. In well-collected areas (e.grand. North America, Europe) and for well-nerveless species, NHCs can provide sufficient information to define historical baselines.
Finally, the value of NHCs can be greatly amplified when integrated with other types of biological data (eastward.1000. physiological, genetic and monitoring information) and when multiple responses are considered simultaneously. The weaknesses of NHC data (east.g. spotty temporal coverage) and its strengths (east.one thousand. long timeframe) are often the perfect complement of the strengths (e.g. yearly data) and weaknesses (e.thousand. short timeframe) of contemporary monitoring studies. Integrated studies with NHCs and the connected long-term monitoring of relevant traits (e.g. trunk size, phenology), as well equally sustained specimen collection and deposition in NHCs [35,70], volition help forecast the futurity of the most various group of animals on Earth.
Acknowledgements
We give thanks the editors for their invitation to contribute to this upshot.
Data accessibility
This article has no additional data.
Authors' contributions
H.Thousand.Thou. and M.V. drafted the outline of the manuscript; all authors wrote and edited the paper; H.M.K., J.Grand.K.L. and J.T.K. produced figures.
Competing interests
We declare we have no competing interests.
Funding
J.Yard.M.L. was supported by a Natural Sciences and Engineering Enquiry Council of Canada Postgraduate Scholarship. H.M.K. was supported by a Natural Sciences and Engineering Research Quango of Canada Discovery Grant.
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