Republic of the Philippines

Central Bicol State University of Agriculture- Sipocot

Impig, Sipocot, Camarines Sur

THE IMPORTANCE OF GENOMIC VARIATION FOR BIODIVERSITY

ECOSYSTEMS AND PEOPLE.

(A REVIEW PAPER)

CAMAING, CHARMAINE R.

CAMINO, GEM ERDY D.

CASTRO, KAREN MAE B.

CENEZA, JOSEPHINE P.

BSED 2-SCIENCE

APRIL 2021
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INTRODUCTION

Humans are altering the composition of biological communities through a

variety of activities that increase rates of species invasions and species

extinctions, at all scales, from local to global. These changes in components of

the Earth's biodiversity cause concern for ethical and aesthetic reasons, but they

also have a strong potential to alter ecosystem properties and the goods and

services they provide to humanity. Ecological experiments, observations, and

theoretical developments show that ecosystem properties depend greatly on

biodiversity in terms of the functional characteristics of organisms present in the

ecosystem and the distribution and abundance of those organisms over space

and time. Species effects act in concert with the effects of climate, resource

availability, and disturbance regimes in influencing ecosystem properties. Human

activities can modify all of the above factors; here we focus on modification of

these biotic controls.

No matter who we are, or where we live, our well-being depends on the

way ecosystems work. Most obviously, ecosystems can provide us with material

things that are essential for our daily lives, such as food, wood, wool and

medicines. Although the other types of benefit we get from ecosystems are easily

overlooked, they can, for example, also play an important role in regulating the

environments in which we live. They can help ensure the flow of clean water and

protect us from flooding or other hazards like soil erosion, land-slips and

tsunamis. They can even contribute to our spiritual well-being, through their
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cultural or religious significance or the opportunities they provide for recreation or

the enjoyment of nature.

Determining and implementing the most effective methods for monitoring

and modifying genetic diversity will require a thorough understanding of not just

allelic variation at specific loci but also epistatic interactions between loci and

genome structure, as well as careful consideration of its population and

community genomic context. The reason for this complexity is that the effects of

a given genetic variant (allele, gene or structural variation) will depend on the

frequencies of alleles at other loci in the individual, the frequencies of those

alleles in the population and the patterns of spatio-temporal co-occurrence

between alleles in interacting species. At present, however, such knowledge is

lacking in most instances, with potentially damaging outcomes (Table 1).

We are writing this review paper in order to improve understanding of how

genetic variation influences the health and well-being of ecosystems and people.

Increasing recognition of the importance of intraspecific genetic (henceforth,

simply ‘genetic’) variation, as well as its contemporary evolution, has led to more

frequent calls for its preservation and also for direct actions to increase current

levels of that variation in natural, captive and domesticated populations.

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Table 1 | Unintentional effects of manipulations to intraspecific variation

Modified organism Effect on interspecific diversity

Petunia Artificial insertion of a maize flower pigmentation

(Petunia hybrids) gene caused its unintended silencing via

hypermethylation of the promoter

Canola Genetically engineered canola fields, engineered to

(Brassica napus) resist herbicide treatment, had lower wild bee

abundance, resulting in a pollination deficit

Bt aspen Insect-resistant Bt aspens caused a change in leaf

(Populus hybrids) litter decomposition that resulted in a shift in the

aquatic insect community

Bt aspen Insect-resistant Bt aspens did not grow larger despite

(Populus hybrids) lesser leaf damage and were still targeted by one

main pest
GH-transgenic coho GH-transgenic salmon, as compared with their non-

salmon transgenic half-siblings, showed more aggressive

(Oncorhynchus foraging behaviour, with differential effects on

kisutch) mortality and foraging success that were contingent

on age 140,141 Bt, Bacillus thuringiensis; GH, growth

hormone.

Bt, Bacillus thuringiensis; GH, growth hormone.

From genes to phenotypes to people

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The benefits of nature (that is, biodiversity) to people are often

conceptualized in terms of ‘ecosystem services’ or ‘nature’s contributions to

people’ (NCP) (box 1). In 2019, the seventh plenary of the IPBES defined 18

categories of NCP (Table 2); these NCP include ecosystem services, and so we

will use the more inclusive term ‘NCP’ throughout this Review. Genetic diversity

influences biodiversity, and thus NCP, in two main ways: (1) through standing

genetic variation (that is, the particular combination of genes and alleles present

at a given time in a given place); and (2) through contemporary evolution (that is,

ongoing evolutionary changes that affect the genetic variation in a given place at

a given time). With respect to standing genetic variation, the underlying idea is

that a particular mix of genetic variants will influence NCP — through the

expressed phenotype — differently from some other mix of genetic variants. With

respect to contemporary evolution, the basic idea is that natural selection and

other evolutionary processes (such as gene flow, mutation and genetic drift) act

on very short time scales to modify the mean and distribution (for example,

variance) of genetically based (that is, heritable) traits that influence NCP.

Box 1 | Ecosystem services and NCP

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MA (2005) IPBES (2013) IPBES (2017)

NATURE NATURE

Biodiversity and Biodiversity and

ECOSYSTEM ecosystem ecosystem

Mother Earth Mother Earth

Nature’s benefits NCP

ES Cultural
to people
context
Supporting Nature’s gift Context-
specific
perspective
Regulating
Regulating Regulating
NCP
ES
Non-material
Cultural NCP
Cultural
ES
Material
NCP
Provisioning
Provisioning Generalizing
ES
perspective

Table 2 | Effects of genetic variation and contemporary evolution on

NCP
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NCP Roles of genetic variation and contemporary

evolution
1 Habitat creation Genetic variation (and its evolution) in important (that is,
and maintenance keystone or foundation) plant species influences many
community and ecosystem properties. For example,
different cottonwood (Populus spp.) genotypes exhibit
different tannin levels and influence the impact of
ecosystem engineers, such as beavers, which forage for
low-tannin variants

Evolution of (or caused by) ecosystem engineers can

change how they shape the environment. For example,
beavers show differential removal of Populus trees with
different tannin genotypes, which has many cascading
influences on riparian ecosystems
2 Pollination and Rapid evolution of plant reproductive systems in
propagule dispersal response to pollinator decline increases plant fitness, as
demonstrated in an experimental study with Mimulus
guttatus

Rapid evolution of dispersal traits in response to habitat

fragmentation. For example, urbanization leads to the
evolution of reduced dispersal in Crepis sancta
3 Regulation of air The role of airborne microorganisms, as well as their
quality evolution and genetic diversity, is currently
underappreciated and understudied
4 Regulation of Rapid evolution of marine phytoplankton increases
climate carbon uptake

Plants and soil microorganisms influence rates of

weathering, which in turn controls CO2 sequestration
and lifetime of CO2 fuel
5 Regulation of Rapid evolution of marine phytoplankton increases
ocean acidification carbon uptake

Rapid evolution of many species facilitates persistence in

the face of increasing acidification
Bt, Bacillus thuringiensis; NCP, nature’s contributions to people.

Genetic diversity and conservation and utilization of plant genetic

resources
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The importance of biodiversity for humankind has been well recognized in

the recent decades and many would argue that diversity is essential for allowing

sustainable development of various human activities. Biological diversity can

enable social and economic systems to flourish in ways that allow the poorest to

meet their food and nutritional needs and retain the cultural diversity of countries

throughout the world (Shiva, 1994). The bio- logical resources of each country

are important, but not all countries are equally endowed, and cooperation

between countries is needed for effective conservation and use of our global

biodiversity. During the past few years there has been increasing awareness of

the importance of adopting a holistic view of biodiversity, including agricultural

biodiversity, and of linking conservation with sustainable utilization and

development (Arora, 1997).

Research needed on genetic diversity extent and distribution

There continues to be a substantial need for research on many aspects of

the extent and distribution of genetic diversity. In respect to the genetic diversity

in useful plant species, there is a particular need to explore the ways in which

farmer management practices and ecological or geographic factors interact to

determine population structure. Is the diversity found in crop populations still

largely explicable in terms of ecogeographic factors and domestication events or

have socio-economic, cultural and political factors had the greatest impact and
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largely minimized the significance of biological or edaphic factors? Research is

also needed on such factors as the distribution of allelic variation within and

between populations, particularly with respect to multi-allelic associations and to

the significance of linkage disequilibrium in determining the importance of linkage

and allelic associations in different crop species. Another key issue with direct

practical implications for conservation management strategies is the extent and

effect of introgression between crop species and their wild relatives (Harris and

Hillman, 1989; Jarvis and Hodgkin, 1999). Research is also needed on the

distribution of allelic variation within and between populations, geographic

patterns of variation as well as and genomically determined allelic associations in

the crops and species concerned along with research on breeding systems. Such

studies will provide valuable information on a number of practical issues of

germplasm management, including the classification of accessions by known

allelic constitution and the detection of redundancy in collections.

The conservation of crop genetic resources can be difficult to sell, but the

stakes are high (Smith and Schultes, 1990). There is pressing need for all those

who are interested in plant genetic resources conservation and use to be more

involved in all the aspects of genetic diversity – to study, understand, enhance,

conserve and use it. To do so, we need to understand the extent and distribution

of diversity in species and ecosystems through appropriate research, field

studies and analysis. Any conservation effort should be an approach that leads to

integrated conservation – a balance of ex situ and in situ methods. There is a

need to stimulate international cooperation or joint ventures on all aspects of

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plant genetic resources. Genetic diversity should be understood at all the three

levels: at the level of species, at the level of genus and at the level of ecosystem.

The major elements that confer value on genetic diversity and its organization

are: the genetic integrity of evolved populations and taxa, or samples of these;

the environments and ecosystems that support both the diversity and its

structure, and its relationship with the ecosystem (Riggs, 1990). The key to

genetic conservation is maintaining and integrating these three elements. To

achieve this we need to improve access to existing knowledge as much as

possible, maintain genetic continuity and integrity wherever possible, and

integrate and coordinate different conservation efforts.

Classic genetic methods to inform NCP

Genetic diversity can be measured using a number of marker genes or

via broader genome-wide approaches. Such analyses can yield ‘proxies’ for

species’ adaptive potential brought about by the varying phenotypes expressed

by that genetic diversity. The vast majority of existing work that investigates

genetic diversity and molecular mechanisms that influence biodiversity

emphasizes simple summary measures of within-population or among-population

single-locus variation (typically averaged across many loci), such as nucleotide

diversity, heterozygosity, allelic richness, allele frequency differences and allele

frequency variance52. Some additional work has focused on quantitative genetic

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measures of within-population variation (for example, additive genetic variance)

or among- population variation, such as Wright’s FST. Similarly simple measures

are used in analyses conducted at the among- species level, with examples

including nucleotide divergence, fixed allele frequency differences and

phylogenetic distance. Such quantifications of genetic diversity are important as

they can support policymakers and conservation programme managers in their

efforts to understand, support and manage NCP. Furthermore, the genetics and

genomics of NCP are in many instances the genetics and genomics of

‘phenotypes’, specifically the association of community and ecosystem

genotypes with expressed community and ecosystem phenotypes, whenever

these phenotypes have emergent effects on the environment. Various

manifestations of this idea include extended phenotypes sensu Dawkins, genes

to ecosystem and interspecific indirect genetic effects. In each instance the

genetic variation at the individual, population or community level is cascading

through the levels of biological organization as opposed to affecting ‘just’

individuals of the same population.

Genotype comparisons
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Classic genetic studies test for phenotypic differences between alternative

genotypes at particular loci, an effort recently made much easier through gene

editing technologies such as CRISPR–Cas9. In the context of NCP, such

methods could be particularly useful for considering ‘ecologically important

genes’, so-called key- stone genes, foundation genes or ecosystem engineering

genes. For example, different cotton- wood (Populus spp.) genotypes exhibit

different tannin levels, which has ecosystem-level effects by affecting soil

microbiota, the arthropod community, plant herbivory and nutrient cycling; they

also influence the impact of ecosystem engineers, such as beavers. Another

example is the evidence that particular genotypes influence the movement of

organisms in ways that have cascading effects for eco- systems and people,

such as genes influencing migration timing in salmonid fishes. For example, wild

chinook salmon from the Rogue River were shown to possess alternative alleles

at the GREB1L locus that determine whether the individuals enter freshwater

streams during the spring or the autumn. The allelic composition within these

populations has been affected by anthropogenic disturbances, ultimately

resulting in genetically impoverished populations that are less resistant to

environmental variability and hence show reduced evolvability. The absence of

salmon that migrate in spring most likely affects entire nutrient cycling pathways

in freshwater streams.
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Genome-wide association studies

Genome-wide analyses seek associations between specific alleles at

particular loci, or multilocus combinations thereof, and qualitative or quantitative

phenotypic differences. These methods could be used to inform NCP if the

‘phenotypes’ of traditional analyses are replaced with the ecological effects of

organisms. As one example, Crutsinger et al. used thousands of SNPs to test for

the genetic basis of the ecological effects (for example, nutrient dynamics in

aquatic habitats) of individual genotypes of riparian trees. They found that

variation in riparian black cottonwood (Populus tri- chocarpa) genotypes from

phenotypically divergent populations results in variable ecosystem traits such as

leaf litter production. This variation in turn affects phytoplankton abundances and

nutrient dynamics, which then affects light availability in neighboring aquatic

habitats. Less light in aquatic habitats negatively feeds back on phytoplankton

and zooplankton abundance, which has large ecological effects up and down the

trophic chain to the predators and prey of the phytoplankton and zooplankton.

Other possibilities could be association mapping of the diets of keystone species

or the behaviors of ecosystem engineers.

Conclusion
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Predicting the effects on NCP of genetic and genomic variation in natural

populations and engineered organisms, as well as the epistatic interactions

within and between individuals, populations and communities, will require the

extensive production of whole-genome data. Fortunately, continual reductions in

cost and time requirements have enabled, and will continue to accelerate,

relevant genomic initiatives.

Indeed, the major limiting step has perhaps now shifted to computational

challenges; yet, these challenges will also lessen with advances in machine

learning, computing power and algorithm speeds. We especially point out the

likely importance of machine learning, which is being applied in population

genomics to calculate population genetic parameters (selection and

demography) from genomic data. Machine learning, especially deep learning,

similarly has great potential in computational ecology where it has recently been

applied to predict species interactions and community assemblies.

Humanity faces many challenges — now and in the years to come — and

our personal and societal responses to those challenges will be a primary

determinant of the futures of biodiversity, ecosystems and people. One set of

responses is sure to revolve around the assessment, monitoring and

manipulation of genetic variation, for two major reasons. First, genetic variation,

and the result- ant phenotypic variation, shapes the interactions between

organisms and their environments, hence being a primary determinant of

organismal responses to future conditions and the role they will play in shaping

future ecological dynamics and NCP. Second, science has reached a watershed
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moment where the ability to quantify genomic variation will soon become nearly

unlimited. We now need to merge these realizations and abilities with a more

holistic view of how nature interacts with people. The definition of NCP by the

IPBES has provided us with unified and well-defined targets, and a common

vocabulary for decision-makers and researchers to identify research targets. To

synergize these efforts to maintain biodiversity, we call for creative collaboration

among geneticists, ecologists, evolutionary biologists, social scientists and

bioinformaticians. The future is not set.

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