Living at the edge, range expansion is a losing battle with mutations

Environments can vary substantially in habitat quality, local population abundance, or carrying capacity. Under some climate change scenarios, new, higher quality habitats become available along the margin of a species’ range (e.g. higher latitudes or altitudes) (Thomas et al 2001). These new habitats may be able to support larger population sizes. Factors of demography, evolution, and qualities of the abiotic and biotic communities all interact to determine where a species is found and may influence the ability of a species to expand its range. New research is building genetically explicit models in order to understand how the interplay of these different factors influence evolutionary changes,

Wordle of Peischl et al 2013

The authors of a recent study focus on how the interaction of the demographic process of range expansion changes the way that natural selection favors beneficial and deleterious mutations (Peischl et al 2013). Using both computer simulations as well as mathematical approximations, the authors find that at the range margins, individuals carry a substantial load of deleterious mutations.

What differs at the margins of an expanding population versus the core? In this case, the authors assumed that the population size and growth rate differed. In the core or center of a population, the number of individuals had reached the carrying capacity of the local environment. There, the population is large and natural selection is efficient at purging deleterious mutations. At the margins, patches are founded with just a few new migrants. That means those patches are starting with very few members and stochastic processes can counter natural selection. While growth rates are high as the local patch swells to carrying capacity, selection is inefficient. Genetic drift weakens the efficiency of natural selection and allows some deleterious mutations to reach fixation in a growing patch. This leads to the pattern of a deleterious mutational load being found at the leading edge of an expanding population. The authors find under various scenarios that this mutational load can persist for a long time and leave a genetic signature within the population.

I found the simulation model as well as the analysis in this paper very accessible. The authors clearly described this unappreciated phenomenon. I was intrigued by what other forces may interact and it led me to ask several questions.

What about dispersal?

This study piqued my curiosity of how dispersal may influence the outcome of natural selection. The dispersal ability of individuals can vary substantially. Dispersal can play an important role in population dynamics, especially under the threat of anthropogenic habitat change (Thomas et al 2004, Williams et al 2008). I am curious about how variation in dispersal affects the interplay of demography and the evolutionary processes.

During any model analysis, it is important to understand the implication of assumptions on the results and how they may provide limitations to interpretation. Population geneticists make a distinction when it comes to incorporating population demography into metapopulations. One distinction is called hard vs. soft selection (Whitlock 2002). Peischl et al (2013) assumed that each local deme, or patch, contributes migrants equally regardless of the local deme fitness. We also refer to this as soft selection. In contrast, it may make sense that demes with a higher local fitness contribute more migrants. This would be an example of what population geneticists call hard selection.

Might the dynamics of the deleterious mutational load be different if the population was assumed to be under hard selection? If the mutational load still accumulates at the range margin, then at some point those patches will have a very low fitness and therefore contribute fewer migrants than they receive. This may result in a slowing of the range expansion. In the long run, the patches at the core, with a higher fitness, may contribute migrants of higher fitness that will weaken the overall mutational load at the margins. Of course, this is just a hypothesis. It is too complicated to just assume my intuition is correct and more analysis is needed. Looking at the code the authors published on Github (https://github.com/CMPG/ADMRE ), it appears they explored this case a bit. I’ll be curious if their future publications explore this effect.

Runaway dispersal

I was curious about exploring dispersal rates that differ across space. Hanski et al. (2004) suggest that newly established populations should have a higher frequency of dispersive individuals in the new habitat. This could lead to an excess of dispersive individuals in a high quality habitat potentially supporting a large population size.

Spatial selection

Spatial selection for increased dispersal at the leading edge of an expanding population. Top: Shown is an individual’s probability of dispersing a particular distance (black line). After dispersal, individuals at the leading edge (green) have dispersed farther than those at the core (orange). Bottom: if individuals breed locally, than the parents of the leading edge produce offspring with a mean dispersal distance that is higher than the core population (dotted green vs black lines). (Adapted from Fig 1 of Phillips et al 2010)

You may ask, what is the mechanism that favors dispersal at the range limits? Intuitively it is easy to understand: individuals and their descendants who made it to the outer edge did so by dispersing there. Phillips et al (2010 and later in Shine et al 2011) describe the process of spatial selection, by which higher dispersal rates are favored at the leading edge of an expanding population.

Importantly, the process of dispersal effectively sorts individuals through space by dispersal ability. That is, individuals on the edge of the expanding population front are at that edge simply because they dispersed farther than other individuals in the population: the process of dispersal has spatially assorted the best dispersers in the population and placed them on the expanding front. Now, because all the best dispersers are in the same place at the same time, they will tend to breed with each other (the ‘‘Olympic Village effect’’). Thus, if any component of dispersal ability is heritable in this hypothetical species, the offspring of the individuals on the front will tend to have higher dispersal ability than the offspring of individuals from the core of the population. (Phillips et al 2010)

Phillips et al even suggest that this Olympic village effect on dispersal could be a runaway evolutionary process.

One famous example of this phenomenon is found among invasive cane toads (Rinella marina) in Australia. In 2006, Phillips et al found that the toads at the leading edge of the expansion had longer legs making them primary candidates for high dispersal capabilities. Later, Lindstrom et al (2013) found (via radio collar measurements) that those toads at the front of the range were more likely to disperse than those at the encamped within the population. Of course, all this getting around comes at a cost. Those long legged toads at the leading edge have been shown to have more spinal injuries (Brown et al 2007).

So the question remains, how might differences in dispersal ability at the range margins effect the outcome of the results form Peischl et al (2013)? Again, one could imagine that higher rates of dispersal at the margins may magnify the effects seen in the paper. Deleterious mutations could surf to fixation on an accelerating wave of expansion. It remains to be seen how this would play out specifically in the model.

Invasive species and phenotypic plasticity

When species encounter novel environments during the course of a range expansion, plastic responses of the phenotype which maintains high fitness across environmental conditions would enhance the chance of persistence. Invasive species offer an excellent natural experiment to study range expansion in modern time scales.  The dynamic process of dispersal across a heterogeneous landscape as well as establishment in locally variable conditions influences the distribution and population genetics of a species (Kinlan and Hastings 2005). Only those individuals that can survive and reproduce once dispersed will lead to actual range expansion.  Therefore, differences in the capacity of populations and individuals to tolerate variable environmental conditions will modify their ability for range expansion. Incorporating the effects described by Peischl et al (2013) could lead to significant new findings.

Stay tuned

This paper presents some exciting new research and it is clear from other publications of this group that they are working on many different questions about evolutionary responses to variable environments (Kirkpatrick and Peischl 2013, Peischl and Kirkpatrick 2012). Be sure to say tuned for future contributions.

REFERENCES

Brown GP, Shilton C, Phillips BL, Shine R (2007) Invasion, Stress, and Spinal Arthritis in Cane Toads. Proceedings of the National Academy of Sciences 104: 17698-17700. DOI: 10.1073/pnas.0705057104

Hanski I, Eralahti C, Kankare M, Ovaskainen O, Siren H (2004) Variation in Migration Propensity among Individuals Maintained by Landscape Structure. Ecology Letters 7: 958-966. DOI: 10.1111/j.1461-0248.2004.00654.x

Kinlan BP, Hastings A (2005) Rates of Population Spread and Geographic Raqnge Expansion: What Exotic Species Tell Us. In: Sax DF, Stachowicz JJ, Gaines SD, editors. Species Invasions: Insights into Ecology, Evolution, and Biogeography. Sunderland, MA: Sinauer. pp. 381-419.

Kirkpatrick M, Peischl S (2013) Evolutionary Rescue by Beneficial Mutations in Environments That Change in Space and Time. Philosophical Transactions of the Royal Society B-Biological Sciences 368: 8. DOI: 10.1098/rstb.2012.0082

Lindström T, Brown GP, Sisson SA, Phillips BL, Shine R (2013) Rapid Shifts in Dispersal Behavior on an Expanding Range Edge. Proceedings of the National Academy of Sciences: DOI: 10.1073/pnas.1303157110

Peischl S, Dupanloup I, Kirkpatrick M, Excoffier L (2013) On the Accumulation of Deleterious Mutations During Range Expansions. Molecular Ecology 22: 5972-5982. DOI: 10.1111/mec.12524

Peischl S, Kirkpatrick M (2012) Establishment of New Mutations in Changing Environments. Genetics 191: 895-U440. DOI: 10.1534/genetics.112.140756

Phillips BL, Brown GP, Webb JK, Shine R (2006) Invasion and the Evolution of Speed in Toads. Nature 439: 803-803. DOI: 10.1038/439803a

Phillips BL, Brown GP, Shine R (2010) Life-History Evolution in Range-Shifting Populations. Ecology 91: 1617-1627. DOI: 10.1890/09-0910.1

Shine R, Brown GP, Phillips BL (2011) An Evolutionary Process That Assembles Phenotypes through Space Rather Than through Time. Proceedings of the National Academy of Sciences 108: 5708-5711. DOI: 10.1073/pnas.1018989108

Simmons AD, Thomas CD (2004) Changes in Dispersal During Species’ Range Expansions. The American Naturalist 164: 378-395. DOI: 10.1086/423430

Thomas CD, Bodsworth EJ, Wilson RJ, Simmons AD, Davies ZG, et al. (2001) Ecological and Evolutionary Processes at Expanding Range Margins. Nature 411: 577-581. DOI: 10.1038/35079066

Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, et al. (2004) Extinction Risk from Climate Change. Nature 427: 145-148. DOI: 10.1038/nature02121

Williams SE, Shoo LP, Isaac JL, Hoffmann AA, Langham G (2008) Towards an Integrated Framework for Assessing the Vulnerability of Species to Climate Change. PLoS Biology 6: e325. DOI: 10.1371/journal.pbio.0060325

Whitlock MC (2002) Selection, Load and Inbreeding Depression in a Large Metapopulation. Genetics 160: 1191-1202.

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