Landscape genetics

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Rivers and mountains can act as barriers to dispersal, thus preventing gene flow between populations. Parque Eagle River, Anchorage, Alaska, Estados Unidos, 2017-09-01, DD 02.jpg
Rivers and mountains can act as barriers to dispersal, thus preventing gene flow between populations.

Landscape genetics is the scientific discipline that combines population genetics and landscape ecology. It broadly encompasses any study that analyses plant or animal population genetic data in conjunction with data on the landscape features and matrix quality where the sampled population lives. This allows for the analysis of microevolutionary processes affecting the species in light of landscape spatial patterns, providing a more realistic view of how populations interact with their environments . [1] Landscape genetics attempts to determine which landscape features are barriers to dispersal and gene flow, how human-induced landscape changes affect the evolution of populations, the source-sink dynamics of a given population, and how diseases or invasive species spread across landscapes. [2]

Contents

Landscape genetics differs from the fields of biogeography and phylogeography by providing information at finer temporal and spatial scales (i.e., at the level of individual genetic variation within a population). Because it focuses on sampling individuals, landscape genetics has the advantage of not having to subjectively define discrete populations prior to analysis. Genetic tools are used to detect abrupt genetic differences between individuals within a population and statistical tools are used to correlate these genetic discontinuities with landscape and environmental features. [3] The results of landscape genetics studies have potentially important applications to conservation biology and land management practices. [3]

History

Landscape genetics emerged as its own discipline after the seminal article entitled "Landscape genetics: combining landscape ecology and population genetics" by Manel et al. appeared in the journal Trends in Ecology and Evolution in 2003. According to that article, the concept that landscape patterns affect how organisms are distributed dates back to the 18th and 19th centuries in the writings of Augustin Pyramus de Candolle and Alfred Russel Wallace. [3] The modern field is interdisciplinary and integrates not only population genetics and landscape ecology, but also the field of spatial statistics. [4] As of 2008, over 655 articles had been published in the field in a variety of genetics and ecological journals. [2]

Map of the McArthur Lake Wildlife Corridor in northern Idaho, United States. It links to adjacent wilderness areas. McArthur Lake Wildlife Corridor sketch map.svg
Map of the McArthur Lake Wildlife Corridor in northern Idaho, United States. It links to adjacent wilderness areas.

Advances and applications

Landscape genetics has advanced ecological and evolutionary theory by facilitating an understanding of how gene flow and adaptation occur in real heterogeneous landscapes. It has also allowed for the estimation of functional connectivity across landscapes. [4] Elucidating landscape features that act as barriers or facilitators of dispersal can inform the construction or preservation of wildlife corridors that connect fragmented landscapes. Landscape genetics can also help predict how diseases will spread across a landscape or how proposed management actions will affect populations. Finally, landscape genetics can help predict how well populations will adapt to continuing global change. [2]

Methods

Genetic markers

Molecular markers of genetic diversity such as DNA microsatellites, mitochondrial DNA, amplified fragment length polymorphisms, and alloenzymes are tested in random individuals of a particular species across a landscape. [2] These markers are used to determine the genotype (genetic make-up) of the individuals tested.

Landscape and environmental features

Landscape features include landscape composition (abundance and variety of patch types), landscape configuration (how these patches are arranged in space), and the quality of the matrix (the space in a landscape between patches of habitat for a given species [5] ). Topography, altitude, habitat types, and potential barriers such as rivers or road are examples of landscape variables. [6]

Statistical tools

Identifying genetic patterns

Various statistical tools are utilized to identify genetic patterns from the genetic markers collected. Methods that cluster individuals into subpopulations based on genetic differentiation or distance, such as fixation index (FST) and Bayesian assignment methods, are often used. However, because individuals are sometimes evenly distributed rather than spatially clustered across a landscape, these methods are limited and alternative methods are being developed. [2]

Correlating genetic patterns to landscape

Statistical tools such as the Mantel test or partial Mantel test are commonly used to correlate genetic patterns with landscape features. Linear regression models and ordination techniques are also common. [2] Geographic information systems (GIS) can be used to visualize genetic patterns across space by plotting genetic data on a map of the landscape. [3]

White tail deer Quintet of White-tailed Deer in a Field, Joy Road ^ Maple Road, Webster Township, Michigan - panoramio.jpg
White tail deer

Example

A study published in 2012 [7] analyzed the landscape genetics of white tail deer in Wisconsin and Illinois.  They extracted DNA from the lymph nodes of 2,069 harvested deer across 64 townships.  Fifteen microsatellite markers were used for genotyping.  A Bayesian population assignment test found no distinct subpopulations based on the genetic data.  Correlograms were used to elucidate fine-scale social structure, and found that more heavily forested and fragmented townships had more genetic relatedness between individual deer.  Spatial principal component analysis was used to elucidate broad-scale population connectivity.  Partial Mantel tests found a correlation between genetic distance and geographic barriers, particularly roads and rivers.  However, these were not absolute barriers and did not divide the deer into distinct subpopulations.

The finding of high genetic connectivity among the sampled deer has management implications for the setting of harvest number and population goals.  The finding of high genetic connectivity also has implications for the spread of chronic wasting disease among deer.

Sub-disciplines

Seascape genetics

Seascape genetics is a sub discipline of landscape genomics that scientists started to use in 2006. [8] The emergence of this field proceeded landscape genetics, advances in genetic laboratory technology, and higher resolution marine environmental data. [9] Like landscape genetics, seascape genetics is a multidisciplinary field. Areas of expertise used in sea scape genetics includes oceanography, ecology, and population genetics. [8] [10] Seascapes differ from landscapes due to differential connectivity in the aquatic environment.  Currents allow for increased connectivity in some locations and restrict connectivity elsewhere. Many organisms that live in the ocean rely on currents to move their gametes and larvae which is called dispersal. Variable dispersal availability leads to subpopulations that have different structure; therefore, subpopulations are exposed to distinct selective pressures, experience separate rates of drift and have unique genetic diversity. [11]

Seascape genomics is a tool that utilizes genetic markers in tandem with current patterns to better understand dispersal. Another key difference when studying marine systems is that many animals have extremely large population sizes. Substantial population sizes in the marine setting allows for greater adaptive potential with larger effective population size, [12] meaning the portion of the population that is reproducing and passing along genes increases. A large population will have greater influence from selection than drift, thus marine organisms are more likely to have greater levels of local adaptation. In seascape analyses, genetic data allows for greater species understanding and tracking when the full life history is unknown or unable to be studied with ecology. [1] Population genetics incorporates many theories and techniques, all of which need to be taken into consideration for seascape and landscape analyses. There are several ways to collect genetic information. Popular methods in seascape genetics have been single nucleotide polymorphisms (SNPs), mitochondrial DNA, random amplified polymorphic DNAs, microsatellites, allozymes, and full genomes. [2] Collecting and processing sufficient samples has been a time-consuming process in the past. Next generation sequencing has helped to expand the field of landscape genomics because it allows for rapid sequencing of extremely large genomes. [13]

Seascape genomics can be applied marine life with varying life histories to answer various questions about genetic influences on population dynamics. Analyzes on sessile organisms, animals such as clams that stay in the same place their whole life, can easily be analyzed to better understand environmental evolutionary pressures. One example, Salmoni et at [14]  used environmental data and genetic analysis to identify a heat tolerant gene in corals. Many other studies have been done on organisms such as oysters, [15] seagrass, [16] and mussels. [17] Motile animals, animals that can move around, have also been studies through seascape genomics. DiBattista and his team [18]  studied how hydrodynamics influences snapper larval disbursement and were able to characterize connectivity between populations. Studies that utilize seascape genomics can be used in conservation and restoration efforts. This type of studies can help to define resilient individuals or classify areas that would be best for marine protected area due to their ecological purpose.

Landscape genomics

Landscape genomics also correlates genetic data with landscape data, but the genetic data comes from multiple loci (locations on a chromosome) across the genome of the organism, as in population genomics. Landscape genetics typically measures less than a dozen different microsatellites in an organism, while landscape genomics often measures single nucleotide polymorphisms at thousands of loci. [19] This allows for the identification of outlier loci that may be under selection. Correlation to landscape data allows for identification of landscape factors contributing to genetic adaptation. This field is growing due to advances in next-generation sequencing techniques. [4]

Pitfalls

As a new and fast growing interdisciplinary field with no explicitly identified best practices, it has been subject to a number of flaws in both study design and interpretation. [20] A 2016 publication [2] identified four common pitfalls of landscape genetics research that should be targeted for correction. These include assuming gene flow is always advantageous, over-generalizing results, failing to consider other processes that affect the genetic structure of populations, and mistaking quantitative methods for robust study design. [20] In particular, authors have been encouraged to report their sampling design, reproducibility of molecular data, and details on the spatial data set and spatial analyses utilized. [2] Because the effects of landscape on gene flow are not universal, sweeping generalities cannot be made, and species-specific studies are necessary. [2]

Many of these pitfalls result from the interdisciplinary nature of landscape genetics, and could be avoided with better collaboration among specialists in the fields of population genetics, landscape ecology, spatial statistics, and geography. [6]

Related Research Articles

<span class="mw-page-title-main">Landscape ecology</span> Science of relationships between ecological processes in the environment and particular ecosystems

Landscape ecology is the science of studying and improving relationships between ecological processes in the environment and particular ecosystems. This is done within a variety of landscape scales, development spatial patterns, and organizational levels of research and policy. Concisely, landscape ecology can be described as the science of "landscape diversity" as the synergetic result of biodiversity and geodiversity.

Phylogeography is the study of the historical processes that may be responsible for the past to present geographic distributions of genealogical lineages. This is accomplished by considering the geographic distribution of individuals in light of genetics, particularly population genetics.

<span class="mw-page-title-main">Gene flow</span> Transfer of genetic variation from one population to another

In population genetics, gene flow is the transfer of genetic material from one population to another. If the rate of gene flow is high enough, then two populations will have equivalent allele frequencies and therefore can be considered a single effective population. It has been shown that it takes only "one migrant per generation" to prevent populations from diverging due to drift. Populations can diverge due to selection even when they are exchanging alleles, if the selection pressure is strong enough. Gene flow is an important mechanism for transferring genetic diversity among populations. Migrants change the distribution of genetic diversity among populations, by modifying allele frequencies. High rates of gene flow can reduce the genetic differentiation between the two groups, increasing homogeneity. For this reason, gene flow has been thought to constrain speciation and prevent range expansion by combining the gene pools of the groups, thus preventing the development of differences in genetic variation that would have led to differentiation and adaptation. In some cases dispersal resulting in gene flow may also result in the addition of novel genetic variants under positive selection to the gene pool of a species or population

<span class="mw-page-title-main">Biological dispersal</span> Movement of individuals from their birth site to a breeding site

Biological dispersal refers to both the movement of individuals from their birth site to their breeding site, as well as the movement from one breeding site to another . Dispersal is also used to describe the movement of propagules such as seeds and spores. Technically, dispersal is defined as any movement that has the potential to lead to gene flow. The act of dispersal involves three phases: departure, transfer, settlement and there are different fitness costs and benefits associated with each of these phases. Through simply moving from one habitat patch to another, the dispersal of an individual has consequences not only for individual fitness, but also for population dynamics, population genetics, and species distribution. Understanding dispersal and the consequences both for evolutionary strategies at a species level, and for processes at an ecosystem level, requires understanding on the type of dispersal, the dispersal range of a given species, and the dispersal mechanisms involved. Biological dispersal can be correlated to population density. The range of variations of a species' location determines expansion range.

<span class="mw-page-title-main">Molecular ecology</span> Field of evolutionary biology

Molecular ecology is a field of evolutionary biology that is concerned with applying molecular population genetics, molecular phylogenetics, and more recently genomics to traditional ecological questions. It is virtually synonymous with the field of "Ecological Genetics" as pioneered by Theodosius Dobzhansky, E. B. Ford, Godfrey M. Hewitt, and others. These fields are united in their attempt to study genetic-based questions "out in the field" as opposed to the laboratory. Molecular ecology is related to the field of conservation genetics.

A null allele is a nonfunctional allele caused by a genetic mutation. Such mutations can cause a complete lack of production of the associated gene product or a product that does not function properly; in either case, the allele may be considered nonfunctional. A null allele cannot be distinguished from deletion of the entire locus solely from phenotypic observation.

Inbreeding depression is the reduced biological fitness that has the potential to result from inbreeding. Biological fitness refers to an organism's ability to survive and perpetuate its genetic material. Inbreeding depression is often the result of a population bottleneck. In general, the higher the genetic variation or gene pool within a breeding population, the less likely it is to suffer from inbreeding depression, though inbreeding and outbreeding depression can simultaneously occur.

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Genetic equilibrium is the condition of an allele or genotype in a gene pool where the frequency does not change from generation to generation. Genetic equilibrium describes a theoretical state that is the basis for determining whether and in what ways populations may deviate from it. Hardy–Weinberg equilibrium is one theoretical framework for studying genetic equilibrium. It is commonly studied using models that take as their assumptions those of Hardy-Weinberg, meaning:

In landscape ecology, landscape connectivity is, broadly, "the degree to which the landscape facilitates or impedes movement among resource patches". Alternatively, connectivity may be a continuous property of the landscape and independent of patches and paths. Connectivity includes both structural connectivity and functional connectivity. Functional connectivity includes actual connectivity and potential connectivity in which movement paths are estimated using the life-history data.

Panmixia means uniform random fertilization. A panmictic population is one where all potential parents may contribute equally to the gamete pool, and that these gametes are uniformally distributed within the gamete population (gamodeme). This assumes that there are no hybridising restrictions within the parental population : neither genetics, cytogenetics nor behavioural; and neither spatial nor temporal. Therefore, all gamete recombination (fertilization) is uniformally possible. Both the Wahlund effect and the Hardy Weinberg equilibrium assume that the overall population is panmictic.

A genetic isolate is a population of organisms with little genetic mixing with other organisms within the same species due to geographic isolation or other factors that prevent reproduction. Genetic isolates form new species through an evolutionary process known as speciation. All modern species diversity is a product of genetic isolates and evolution.

Genetic monitoring is the use of molecular markers to (i) identify individuals, species or populations, or (ii) to quantify changes in population genetic metrics over time. Genetic monitoring can thus be used to detect changes in species abundance and/or diversity, and has become an important tool in both conservation and livestock management. The types of molecular markers used to monitor populations are most commonly mitochondrial, microsatellites or single-nucleotide polymorphisms (SNPs), while earlier studies also used allozyme data. Species gene diversity is also recognized as an important biodiversity metric for implementation of the Convention on Biological Diversity.

<span class="mw-page-title-main">Isolation by distance</span>

Isolation by distance (IBD) is a term used to refer to the accrual of local genetic variation under geographically limited dispersal. The IBD model is useful for determining the distribution of gene frequencies over a geographic region. Both dispersal variance and migration probabilities are variables in this model and both contribute to local genetic differentiation. Isolation by distance is usually the simplest model for the cause of genetic isolation between populations. Evolutionary biologists and population geneticists have been exploring varying theories and models for explaining population structure. Yoichi Ishida compares two important theories of isolation by distance and clarifies the relationship between the two. According to Ishida, Sewall Wright's isolation by distance theory is termed ecological isolation by distance while Gustave Malécot's theory is called genetic isolation by distance. Isolation by distance is distantly related to speciation. Multiple types of isolating barriers, namely prezygotic isolating barriers, including isolation by distance, are considered the key factor in keeping populations apart, limiting gene flow.

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References

  1. 1 2 Holderegger, Rolf; Wagner, Helene H. (2006-08-01). "A brief guide to Landscape Genetics". Landscape Ecology. 21 (6): 793–796. doi:10.1007/s10980-005-6058-6. ISSN   1572-9761. S2CID   5769696.
  2. 1 2 3 4 5 6 7 8 9 10 Storfer, Andrew; Murphy, Melanie A.; Spear, Stephen F.; Holderegger, Rolf; Waits, Lisette P. (2010). "Landscape genetics: where are we now?". Molecular Ecology. 19 (17): 3496–3514. doi: 10.1111/j.1365-294X.2010.04691.x . ISSN   1365-294X. PMID   20723061.
  3. 1 2 3 4 Manel, Stephanie; Schwartz, Michael K; Luikart, Gordon; Taberlet, Pierre (2003-04-01). "Landscape genetics: combining landscape ecology and population genetics". Trends in Ecology & Evolution. 18 (4): 189–197. doi:10.1016/S0169-5347(03)00008-9. ISSN   0169-5347.
  4. 1 2 3 Manel, Stephanie; Holderegger, Rolf (2013-10-01). "Ten years of landscape genetics". Trends in Ecology & Evolution. 28 (10): 614–621. doi:10.1016/j.tree.2013.05.012. ISSN   0169-5347. PMID   23769416.
  5. ↑ Wagner, Helene H.; Holderegger, Rolf (2008-03-01). "Landscape Genetics". BioScience. 58 (3): 199–207. doi: 10.1641/B580306 . hdl: 1807/75562 . ISSN   0006-3568.
  6. 1 2 Storfer, A; Murphy, MA; Evans, JS; Goldberg, CS; Robinson, S; Spear, SF; Dezzani, R; Delmelle, E; Vierling, L (2007). "Putting the 'landscape' in landscape genetics". Heredity. 98 (3): 128–142. doi: 10.1038/sj.hdy.6800917 . ISSN   1365-2540. PMID   17080024.
  7. ↑ Robinson, Stacie J.; Samuel, Michael D.; Lopez, Davin L.; Shelton, Paul (2012). "The walk is never random: subtle landscape effects shape gene flow in a continuous white-tailed deer population in the Midwestern United States". Molecular Ecology. 21 (17): 4190–4205. doi:10.1111/j.1365-294X.2012.05681.x. ISSN   1365-294X. PMID   22882236. S2CID   17905176.
  8. 1 2 Selkoe, KA; D’Aloia, CC; Crandall, ED; Iacchei, M; Liggins, L; Puritz, JB; von der Heyden, S; Toonen, RJ (2016-07-28). "A decade of seascape genetics: contributions to basic and applied marine connectivity". Marine Ecology Progress Series. 554: 1–19. doi: 10.3354/meps11792 . hdl: 10179/17416 . ISSN   0171-8630.
  9. ↑ Liggins, Libby; Treml, Eric A.; Riginos, Cynthia (2019), "Seascape Genomics: Contextualizing Adaptive and Neutral Genomic Variation in the Ocean Environment", Population Genomics, Cham: Springer International Publishing, pp. 171–218, doi:10.1007/13836_2019_68, ISBN   978-3-030-37935-3, S2CID   213340840 , retrieved 2022-11-21
  10. ↑ Holderegger, Rolf; Wagner, Helene H. (2008-03-01). "Landscape Genetics". BioScience. 58 (3): 199–207. doi: 10.1641/b580306 . hdl: 1807/75562 . ISSN   1525-3244. S2CID   198156341.
  11. ↑ Balkenhol, Niko; Dudaniec, Rachael Y.; Krutovsky, Konstantin V.; Johnson, Jeremy S.; Cairns, David M.; Segelbacher, Gernot; Selkoe, Kimberly A.; von der Heyden, Sophie; Wang, Ian J. (2017), "Landscape Genomics: Understanding Relationships Between Environmental Heterogeneity and Genomic Characteristics of Populations", Population Genomics, Cham: Springer International Publishing, pp. 261–322, doi:10.1007/13836_2017_2, ISBN   978-3-030-04587-6 , retrieved 2022-11-21
  12. ↑ Riginos, Cynthia; Crandall, Eric D.; Liggins, Libby; Bongaerts, Pim; Treml, Eric A. (2016-07-06). "Navigating the currents of seascape genomics: how spatial analyses can augment population genomic studies". Current Zoology. 62 (6): 581–601. doi:10.1093/cz/zow067. ISSN   1674-5507. PMC   5804261 . PMID   29491947.
  13. ↑ Rellstab, Christian; Gugerli, Felix; Eckert, Andrew J.; Hancock, Angela M.; Holderegger, Rolf (2015-08-26). "A practical guide to environmental association analysis in landscape genomics". Molecular Ecology. 24 (17): 4348–4370. doi: 10.1111/mec.13322 . ISSN   0962-1083. PMID   26184487. S2CID   27067681.
  14. ↑ Selmoni, Oliver; Lecellier, Gaël; Magalon, Hélène; Vigliola, Laurent; Benzoni, Francesca; Peignon, Christophe; Joost, Stéphane; Berteaux-Lecellier, Véronique (2020-05-12). "Seascape genomics reveals candidate molecular targets of heat stress adaptation in three coral species". doi: 10.1101/2020.05.12.090050 . hdl: 10754/667637 . S2CID   218644018.{{cite journal}}: Cite journal requires |journal= (help)
  15. ↑ Bernatchez, Simon; Xuereb, Amanda; Laporte, Martin; Benestan, Laura; Steeves, Royce; Laflamme, Mark; Bernatchez, Louis; Mallet, Martin A. (2018-12-26). "Seascape genomics of eastern oyster (Crassostrea virginica) along the Atlantic coast of Canada". Evolutionary Applications. 12 (3): 587–609. doi: 10.1111/eva.12741 . ISSN   1752-4571. PMC   6383708 . PMID   30828376. S2CID   67862683.
  16. ↑ Jahnke, Marlene; Jonsson, Per R.; Moksnes, Per-Olav; Loo, Lars-Ove; Nilsson Jacobi, Martin; Olsen, Jeanine L. (2018-01-26). "Seascape genetics and biophysical connectivity modelling support conservation of the seagrassZostera marinain the Skagerrak-Kattegat region of the eastern North Sea". Evolutionary Applications. 11 (5): 645–661. doi:10.1111/eva.12589. ISSN   1752-4571. PMC   5979629 . PMID   29875808.
  17. ↑ Wei, K; Wood, AR; Gardner, JPA (2013-03-12). "Seascape genetics of the New Zealand greenshell mussel: sea surface temperature explains macrogeographic scale genetic variation". Marine Ecology Progress Series. 477: 107–121. doi: 10.3354/meps10158 . ISSN   0171-8630.
  18. ↑ DiBattista, Joseph D.; Travers, Michael J.; Moore, Glenn I.; Evans, Richard D.; Newman, Stephen J.; Feng, Ming; Moyle, Samuel D.; Gorton, Rebecca J.; Saunders, Thor; Berry, Oliver (2017-10-28). "Seascape genomics reveals fine-scale patterns of dispersal for a reef fish along the ecologically divergent coast of Northwestern Australia". Molecular Ecology. 26 (22): 6206–6223. doi:10.1111/mec.14352. hdl: 20.500.11937/59488 . ISSN   0962-1083. PMID   29080323. S2CID   3497247.
  19. ↑ Storfer, Andrew; Patton, Austin; Fraik, Alexandra K. (2018). "Navigating the Interface Between Landscape Genetics and Landscape Genomics". Frontiers in Genetics. 9: 68. doi: 10.3389/fgene.2018.00068 . ISSN   1664-8021. PMC   5859105 . PMID   29593776.
  20. 1 2 Richardson, Jonathan L.; Brady, Steven P.; Wang, Ian J.; Spear, Stephen F. (2016). "Navigating the pitfalls and promise of landscape genetics". Molecular Ecology. 25 (4): 849–863. doi: 10.1111/mec.13527 . ISSN   1365-294X. PMID   26756865. S2CID   23647434.
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