The evolution of invasive species

Invasion success is determined both by the evolution of the invader and the species in the invaded community. Here we are interested only in evolution of characteristics that promote the success of NIS.

The usual conditions of invasion (i.e. small initial population size of non-indigenous species, etc.) make possible rapid evolution of these species.

However, that is ‘putting the cart before the horse’. Invasion is a multi-stage process. Each stage acts as a selective filter, and we need to consider evolution as it relates to each stage. What are those stages?

1. Evolution in the native range (pre-adaptation).

2. Evolution related to transport from native to invaded habitats.

3. Evolution in the invaded habitat during introduction, establishment and spread.

In part, this relates to the filter model you’ve already seen. That model does not consider pre-adaptation; it assumes the evolved characteristics of the species is suitable for invasion. In addition, it subdivides stage 3, separating the filters related to evolved physiology from the relationship the invader has to the invaded community.

Model to Predict Invasions

Species Pool A B C D E F G

Transport (Dispersal) Filter

Physiological Filter (+/-)

Biotic Filter (+/-)

ENatural Colonization

you must get there

you must survive conditions

you must tolerate species already present

Pre-adaptation

Invasive species are not a random group from within native biodiversity. Their evolved traits predispose them to transport (particularly human-mediated transport) from native to invaded habitats.

What are those traits?

high fecundity small body size vegetative or asexual reproduction high genetic diversity high phenotypic plasticity physiological tolerance

High fecundity (and regular reproduction) produces high propagule pressure.

Small body size (and usually small propagule size or seed mass) means that maturity can be reached rapidly, and makes it more likely that high fecundity can be achieved.

The regularity of reproduction (and/or short reproductive interval) means that additional propagules are likely dispersed to an invaded habitat after first arrivals. That reduces possibly harmful Allee effects, increases genetic diversity in the novel habitat, and permits adaptive evolution in that habitat.

High genetic diversity in the native range means that even a small initial population in the invaded habitat can produce a broad range of genotypes and phenotypes in the invaded area.

Reproductive strategies of invasive plant species frequently involve extensive vegetative reproduction and/or asexual reproduction or self-fertility. Any of these approaches minimizes the requirement for mates within a local area.

Broad physiological tolerance in the native habitat means that a potential invader is less likely to be filtered out by environmental conditions in the invaded habitat.

The same end point can be achieved by phenotypic plasticity.

Either of the above likely means we would identify the species as being a habitat generalist in its native range.

Examples:

Pines (Pinus)

Rejmanek and Richardson (1996) separated species of pines into invasive and non-invasive groups. They performed a discriminant analysis on data that included various biological characteristics of the species. The discriminant function that best separated the groups included: seed mass, interval between large seed crops and minimum juvenile period.

What about other plant species? Rejmanek and Richardson found they could use the same basic characteristics and add the potential for vertebrate seed dispersal to produce a more general pattern for what species are likely to be invasive:

Here the Z is their discriminant function score:

Positive Z scores in the discriminant analysis are an indication the species is invasive; negative Z scores occur in non-invasive species.

Pinus contorta – an invasive speciesCommon name: lodgepole pineDistribution:southeastern Alaska to northern California, Sierra Nevada, Rocky Mts, Black HillsNeedles: 3-4 cmSeeds: 1-2 mm, wings to 12 mm

Pinus engelmanii – non-invasiveCommon name: Aztec pineDistribution: northern Mexico, Arizona, New MexicoSeed size: 8-9 mm circumference, wings to 20 mmNeedles: 8-14 inches

Insects – in particular a walnut husk fly, Rhagoletis completa

Here we have an example that points to the value of both genetic diversity and a ‘general purpose genotype’ (which might be either a species with broad physiological tolerance or phenotypic plasticity).

We might expect a new invader to suffer a genetic bottleneck on invasion. Limited genetic diversity could inhibit success. However, there are two ways an invasive population could be successful:

1. An invader could very rapidly be selected for local adaptations. This would depend on sufficient local genetic diversity (e.g. by multiple invasions) – or –

2. If invasive species show “general-purpose genotypes”, or display sufficient phenotypic plasticity to thrive under a wide range of environmental conditions.

R. completa apparently took advantage of both approaches…

Colonization of California walnut groves apparently occurred repeatedly and sequentially from midwestern sources. Checks of microsatellite genetic diversity in California do not indicate a significant bottleneck. – and –

Even though there is a significant difference in climate between California and midwestern source areas, there was no significant difference in diapausecharacteristics, normally induced by climatic conditions. The flies carry either a very large phenptypic plasticity and/or a very general purpose genotype.

Table 1 Rhagoletis completa populations used in the studyLocation Mean number of alleles Total number of alleles Heterozygosity

Introduced

Wapato, Washington 4.83 29 0.57 0.33

Medford, Oregon 4.67 28 0.51 0.29

Lakeport, California 4.50 27 0.50 0.29

Lodi, California 4.33 26 0.49 0.29

Hollister, California 4.17 25 0.46 0.27

Tulare , California 3.17 19 0.49 0.29

Native

Columbia, Missouri 3.83 23 0.48 0.28

Blackjack, Missouri 5.00 30 0.53 0.31

Kerrville, Texas 5.17 31 0.54 0.31

Austin, Texas 4.83 29 0.53 0.31

Diapause length was shorter in introduced populations in both California and the midwest, but climate difference did not significantly affect the response. Instead, finding the same response suggests there may be rapid local adaptation, but certainly a ‘general purpose genotype’.

Evolution related to transport

Any change that increases propagule pressure would enhance the probability of successful invasion. Evolutionary changes related to this phase seem less well studied.

The number of propagules per reproductive episode could be increased.

The interval between reproductive episodes could be shortened or more regular.

The nature or quality of dispersal accessory structures or attractiveness to vectors could be enhanced.

Evolution in the introduced range

There is typically a more-or-less extended ‘lag’ phase in population size after introduction. That could be just a typical growth response, but is suggested more likely a result of adaptive evolution following introduction.

The usually accepted hypothesis of founder effects and reduced genetic diversity at introduction seem not to be supported by data. Wares et al. (2005) found invading animal species (29 species reported) retain 80% of the genetic diversity of their native source populations. Bottlenecks, where they occur, seem to be short-lived.

After invasion we expect genetic changes in the invading populations.

What types of genetic change are frequently observed?

1. hybridization, particularly among individuals introduced from different sources. Looking back to Chen’s study of Rhagoletis, some introduced populations had greater genetic diversity than any of the native ones. This, she believes, was due to hybridizations among multiple invasions.

Interspecific hybridization might also occur between introduced and similar native species.

Combinations can also lead to new phenotypes (novel multi-locus genotypes: Novak 2007) and novel epistatic interactions.

2. Another way to produce new genetic variants is through chromosomal or gene duplication. Multiple copies make possible novel adaptive traits.

3. One way of achieving rapid growth (and thus avoiding inbreeding depression or bottlenecks during early phases of invasion) available to plants is uniparental reproduction: selfing, asexual reproduction by clonal propagation and apomixis). These may be pre-adaptations or -

Selection on invading plant species seems to lead to loss of mating types in species with polymorphic systems. Some species shift to obligate asexuality in various ways – clonal propagation and selfing have been reported in evolution of invading populations.

Barrett and his collaborators have discovered loss of morphs in tristylous Eichornia crassipes. Recessive modifiers that appear in founder populations have been shown responsible for evolution of selfing.

ReferencesBarrett, S.C.H., R.I.Colautti and C.G.Eckert. 2008. Plant reproductive systems and evolution during biological invasion. Molecular Ecology 17:373-383.

Chen, Y.H., S.B.Opp, S.H.Berlocher and G.K.Roderick. 2006. Are bottlenecks associated with colonization? Genetic diversity and diapause variation of native and introduced populations Rhagoletis completa populations. Oecologia 149:656-667.

Novak, S.J. 2007. The role of evolution in the invasion process. PNAS 104:3671-2.

Rejmanek, M. and D.M.Richardson. 1996. What attributes make some plant species more invasive? Ecology 77:1655-1661.

Sax, D.F., J.J. Stachowicz and S.D. Gaines (eds). 2005. Species Invasions – Insights into Ecology, Evolution and Biogeography. Sinauer, Sunderland, MA. 495p.

Suarez, A.V. and N.D.Tsutsui. 2008. The evolutionary consequences of biological invasions. Molecular Ecology 17:351-360.