Phenotypic evolution during range expansions is contingent on connectivity and density dependence
Landscape connectivity alters the evolution of density-dependent dispersal during pushed range expansions
Understanding the mechanisms underlying range expansions is key for predicting species distributions in response to environmental changes (such as global warming) and managing the global expansion of invasive species (Parmesan 2006; Suarez & Tsutsui 2008). Traditionally, two types of ecological processes were studied as essential in shaping range expansion: dispersal and population growth. However, ecology and evolution are intertwined in range expansions, as phenotypic evolution of traits involved in demographic and dispersal patterns and processes can affect and be affected by ecological dynamics, representing a full eco-evolutionary loop (Williams et al. 2019; Miller et al. 2020).
Range expansions can be characterized by the type of population growth and dispersal, divided into pushed or pulled range expansions. Species that have high dispersal and high population growth at low densities present pulled range expansions (pulled by individuals from the edge populations). In contrast, populations presenting increased growth rate at intermediate densities (due to Allee effects - Allee & Bowen 1932; i.e. where growth rate decreases at lower densities) and high dispersal at high densities present pushed range expansions (driven by individuals from core and intermediate populations) (Gandhi et al. 2016). Importantly, the type of expansion is expected to have very different consequences on the genetic (and therefore) phenotypic composition of core and edge populations. Specifically, genetic variability is expected to be lower in populations experiencing pulled expansions and higher in populations involved in pushed expansions (Gandhi et al. 2016; Miller et al. 2020). However, it is not always possible to distinguish between pulled and pushed expansions, as variation in speed and shape can overlap between the two types. In addition, it is difficult to experimentally manipulate the strength of the Allee effect to create pushed versus pulled expansions. Thus, several critical predictions regarding the genetic and phenotypic composition of pulled and pushed expansions are lacking empirical tests (but see Gandhi et al. 2016).
In a previous study, Dahirel et al. (2021a) combined simulations and experimental evolution of the small wasps Trichogramma brassicae to show that low connectivity led to more pushed expansions, and higher connectivity generated more pulled expansions. In accordance with theoretical predictions, this led to reduced genetic diversity in pulled expansions, and the reverse pattern in pushed expansions. However, the question of how pulled and pushed expansions affect trait evolution remained unanswered.
In this follow-up study, Dahirel et al. (2021b) tackled this issue and linked the changes in connectivity and type of expansion with the phenotypic evolution of several traits using individuals from their previous experiment. Namely, the authors compared core and edge populations with founder strains to test how evolution in pushed vs. pulled expansions affected wasp size, short movement, fecundity, dispersal, and density dependent dispersal. When density dependence was not accounted for, phenotypic changes in edge populations did not match the expectations from changes in expansion dynamics. This could be due to genetic trade-offs between traits that limit phenotypic evolution (Urquhart & Williams 2021).
However, when accounting for density dependent dispersal, Dahirel et al. (2021b) observed that more connected landscapes (with pulled expansions) showed positive density dispersal in core populations and negative density dispersal in edge populations, similarly to other studies (e.g. Fronhofer et al. 2017). Interestingly, in pushed (with lower connectivity) landscapes, such shift was not observed. Instead, edge populations maintained positive density dispersal even after 14 generations of expansion, whereas core populations showed higher dispersal at lower density. The authors suggest that this seemingly contradictory result is due to a combination of three processes: 1) the expansion reduced positive density dispersal in edge populations; 2) reduced connectivity directly increased dispersal costs, increasing high density dispersal; and 3) reduced connectivity indirectly caused demographic stochasticity (and reduced temporal variability in patches) leading to higher dispersal at low density in core populations. However, these results must be taken with a grain of salt, since only one of the four experimental replicates were used in the density dependent dispersal experiment. In range expansions experiments, replication is fundamental, since stochastic processes (such as gene surfing, where alleles maybe rise in frequency due by chance) are prevalent (Miller et al. 2020), and results are highly dependent on sample size, or number of replicate populations analysed.
Having said that, results from Dahirel et al. (2021b) highlight the importance to contextualize the management of invasions and species distribution, since it is thought that pulled expansions are more prevalent in nature, but pushed expansions can be more important in scenarios where patchiness is high, such as urban landscapes. Moreover, Dahirel's et al. (2021b) study is a first step showing that accounting for trait density dependence is crucial when following phenotypic evolution during range expansion, and that evolution of density dependent traits may be constrained by landscape conditions. This highlights the need to account for both connectivity and density dependence to draw more accurate predictions on the evolutionary and ecological outcomes of range expansions.
Allee WC, Bowen ES (1932) Studies in animal aggregations: Mass protection against colloidal silver among goldfishes. Journal of Experimental Zoology, 61, 185–207. https://doi.org/10.1002/jez.1400610202
Dahirel M, Bertin A, Calcagno V, Duraj C, Fellous S, Groussier G, Lombaert E, Mailleret L, Marchand A, Vercken E (2021a) Landscape connectivity alters the evolution of density-dependent dispersal during pushed range expansions. bioRxiv, 2021.03.03.433752, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2021.03.03.433752
Dahirel M, Bertin A, Haond M, Blin A, Lombaert E, Calcagno V, Fellous S, Mailleret L, Malausa T, Vercken E (2021b) Shifts from pulled to pushed range expansions caused by reduction of landscape connectivity. Oikos, 130, 708–724. https://doi.org/10.1111/oik.08278
Fronhofer EA, Gut S, Altermatt F (2017) Evolution of density-dependent movement during experimental range expansions. Journal of Evolutionary Biology, 30, 2165–2176. https://doi.org/10.1111/jeb.13182
Gandhi SR, Yurtsev EA, Korolev KS, Gore J (2016) Range expansions transition from pulled to pushed waves as growth becomes more cooperative in an experimental microbial population. Proceedings of the National Academy of Sciences, 113, 6922–6927. https://doi.org/10.1073/pnas.1521056113
Miller TEX, Angert AL, Brown CD, Lee-Yaw JA, Lewis M, Lutscher F, Marculis NG, Melbourne BA, Shaw AK, Szűcs M, Tabares O, Usui T, Weiss-Lehman C, Williams JL (2020) Eco-evolutionary dynamics of range expansion. Ecology, 101, e03139. https://doi.org/10.1002/ecy.3139
Parmesan C (2006) Ecological and Evolutionary Responses to Recent Climate Change. Annual Review of Ecology, Evolution, and Systematics, 37, 637–669. https://doi.org/10.1146/annurev.ecolsys.37.091305.110100
Suarez AV, Tsutsui ND (2008) The evolutionary consequences of biological invasions. Molecular Ecology, 17, 351–360. https://doi.org/10.1111/j.1365-294X.2007.03456.x
Urquhart CA, Williams JL (2021) Trait correlations and landscape fragmentation jointly alter expansion speed via evolution at the leading edge in simulated range expansions. Theoretical Ecology. https://doi.org/10.1007/s12080-021-00503-z
Williams JL, Hufbauer RA, Miller TEX (2019) How Evolution Modifies the Variability of Range Expansion. Trends in Ecology & Evolution, 34, 903–913. https://doi.org/10.1016/j.tree.2019.05.012
Inês Fragata (2021) Phenotypic evolution during range expansions is contingent on connectivity and density dependence . Peer Community in Evolutionary Biology, 100133. https://doi.org/10.24072/pci.evolbiol.100133
Evaluation round #2
DOI or URL of the preprint: https://doi.org/10.1101/2021.03.03.433752
Version of the preprint: 3
Author's Reply, 13 Sep 2021
Decision by Inês Fragata, 13 Sep 2021
I think this version is now much clearer in how it differs from other works and how it is actually pushing the field forward, as well as on the limitations that it has. I really like the overview figure and it was much easier to follow up the different experiments and the generations they were performed.
I have one medium comment and several minor suggestions/comments, almost exclusively on the writing. Once these are addressed, I will be happy to write the recommendation!
My biggest comment is that the first paragraph of the introduction (L36 to L44) is a bit disconnected. I could not follow the reasoning behind it.
L36: Maybe start with: “The distribution ranges for many species are …”
L37-38: This sentence is a bit disconnected from the first, because it is not clear what the “their dynamics “referes to? is it the range expansion dynamics?
L43: is likely key --> is important (there are several citations backing up this importance!)
L83-85: Maybe rephrasing the beginning of the sentence might help: “The position of a range expansion on the push-pulled continuum…”
L88: exploring this is in our opinion the --> exploring this is, in our opinion, the
L89: given the distinction --> given that the distinction
L94: rephrase the beginning to: The few (theoretical and empirical) studies focusing on this subject hint that….
L123- 124: Maybe something like: “Using this data we examine the phenotypic changes underlying the different types of range expansions, in space and time.”
L185 – Really cool figure 2!
L223: (except one where this was 15) --> (except one with only 15)
L252: complementary from short-term --> complementary to the short-term
L253: as while --> since
L254: behaviour, this --> behaviour, and this
L272: were this time manipulated --> were manipulated
L289-290: data in a bayesian --> data using a bayesian
L295: warm-up iterations--> burn-in iterations
Also please add the number (or interval) of burn-in iterations used in general
L384: Moving to the effect of rearing density--> Additionally, fecundity was not (…)
L389: There was no such density --> There was no density
L391: experimental landscapes are in almost --> experimental landscapes were in almost
L404: before --> previously
L434: remove the from “the trade-offs”
L436: Add commas “may reduce and in some cases prevent” --> may reduce, and in some cases prevent,
L438: matter a lot to --> may be key to
L440: Whether or not trade-offs matter--> Irrespective of the impact of trade-offs,
452: led to the appearance of a link --> showed/ suggested/ indicated a link
L465: there is actually
L477: Start the sentence with the however and remove it from the middle of the sentence and add a that after given.
However, it is difficult to say whether (..) range expansions, given that many dispersal models (..)
L481: show that shifts
L487 – 490: I would revert the order of the sentence:
Our results at the expanding edge are consistent with existing theory, since strong enough increases (…)
L490-491: Start with however: “However, in core populations dispersal became (…)”
L517: Separate the sentences: “life histories. Further “
518: would be better equipped --> would be important
Evaluation round #1
DOI or URL of the preprint: https://doi.org/10.1101/2021.03.03.433752
Version of the preprint: 2
Author's Reply, 23 Apr 2021
Decision by Inês Fragata, 23 Apr 2021
Your work has been assessed by three reviewers and me. Whereas we generally agree that the work is very interesting and clearly has an added value to the study of the eco-evolutionary dynamics of range expansion, there are some changes that would improve the current manuscript and are needed to clarify some aspects of your experimental design.
### General comments
I think that the manuscript is very interesting and relevant, but there are several things that need to be improved. Reviewers 1 and 2 provide several comments that will allow you to do this. I am adding below comments of my own, with the intent of also helping on this matter. I think the supplementary material is great!
### Specific comments
As reviewer 1 stated there are some literature, especially theoretical, that can be added to the introduction and later on discussed (reviewer 1 provides most of these examples).
Some additional references that may (or not) be of use also:
- Miller TEX, Angert AL, Brown CD, Lee-Yaw JA, Lewis M, Lutscher F, Marculis NG, Melbourne BA, Shaw AK, Szűcs M, Tabares O, Usui T, Weiss-Lehman C, Williams JL. Eco-evolutionary dynamics of range expansion. Ecology. 2020 Oct;101(10):e03139. doi: 10.1002/ecy.3139. Epub 2020 Sep 2. PMID: 32697876.
- Zaker N, Ketchemen L, Lutscher F. The Effect of Movement Behavior on Population Density in Patchy Landscapes. Bull Math Biol. 2019 Dec 23;82(1):1. doi: 10.1007/s11538-019-00680-3. PMID: 31919597.
- Williams, J.L. and Levine, J.M. (2018), Experimental evidence that density dependence strongly influences plant invasions through fragmented landscapes. Ecology, 99: 876-884. https://doi.org/10.1002/ecy.2156
- Urquhart, C.A., Williams, J.L. Trait correlations and landscape fragmentation jointly alter expansion speed via evolution at the leading edge in simulated range expansions. Theor Ecol (2021). https://doi.org/10.1007/s12080-021-00503-z
You should add a figure that explains better your experimental design (i.e. how many strains and replicates per strain x type of connectivity you have) and also a table explaining which traits were sampled in each generation and which replicates from each population were used. I think this is a really important piece of information that you need to add to the manuscript, it was super confusing to understand what you did in each generation and knowing that you selected a replicate at random was not helpful at all.
Another important piece of information that you should is also the size of the landscapes (i.e. the number of patches). This information is available in your initial paper, but I think it should also be here.
In your analyses, have you considered using the number of the edge patch as a covariate? I am assuming that different landscapes had different sizes. If so, adding the expansion size as covariate (or the number of the edge patch were you took the individuals from) allows to test if the several traits analysed were in some way correlated to how much the population expanded.
Another suggestion that I have is to do a multivariate analysis with all traits assuming that, in general, you used the same replicate population across time (and with the BIG caution note that the traits were analysed in different generations). This is because invasive populations often have the invasion syndrome and I wonder if here, by checking each trait individually, you might miss the sign. I know this is more unconventional, so really up to you to see whether this makes sense in your system.
Please clarify why do you use two measures of dispersal.
In line with reviewer 1, I find the use of the word context very confusing, as it can relate to different things. I think that you should specify the comparisons you are doing and not give a general nomenclature (both here and in the results).
In your analyses have you nested experimental replicate in the interaction between experimental landscape and strain? This will be important to guarantee the level at which the intercept is varying.
You should use more precise language in the description of the results.
To improve plot readability on all figures, I would put a line to mark the median value of the stock populations (like you do in fig 4C) across all other facets in the plot. This way the comparison between stock and the evolved populations would be easier. In addition, it will also make it easier to see how different the two evolved populations are from each other.
I think the discussion needs to incorporate a bit more some predictions from theoretical studies. I think that it would be great if you add some of predictions to the introduction and then revisit them in the discussion, to give a greater depth to these results.
As reviewer 2 pointed out, beware the fact that you only analyzed one single replicate for some traits, which limits your ability to generalize your results.
L374: 376 – The sentence staring by “This is despite...” is a bit confusing, i am not sure if it is a comma missing or the structure of the sentence that is not correct.
L439:441 - The sentence staring by “By contrast...” is also a bit weirdly phrased