Understanding Maladaptation by Uniting Ecological and Evolutionary Perspectives

Brady, Steven P.; Bolnick, Daniel I.; Barrett, Rowan D. H.; Chapman, Lauren J.; Crispo, Erika; Derry, Alison M.; Eckert, Christopher G.; Fraser, Dylan J.; Fussmann, Gregor F.; Gonzalez, Andrew; Guichard, Frédéric; Lamy, Thomas; Lane, Jeffrey E.; McAdam, Andrew G.; Newman, Amy E. M.; Paccard, Antoine; Robertson, Bruce A.; Rolshausen, Gregor; Schulte, Patricia M.; Simons, Andrew M.; Vellend, Mark; Hendry, Andrew P.

doi:10.1086/705020

Cited by 65 publications

(65 citation statements)

References 222 publications

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“…The number of colonizers has been shown to play an important role in adaptation: an increase in the number of immigrants helps populations to adapt to new habitats via genetic and demographic rescue (Alzate et al , Peniston et al ), but a further increase has a detrimental effect due to genetic load (Alzate et al , Peniston et al ). An increase in propagule frequency might benefit non‐preadapted populations (but not too high as this leads to maladaptation, see Brady et al , b for a review on causes and definitions of maladaptation), whereas, it might harm preadapted population (by turning them maladapted). If the immigrants are preadapted, an increase in propagule pressure might benefit non‐preadapted populations.…”

Section: Discussionmentioning

confidence: 99%

The role of preadaptation, propagule pressure and competition in the colonization of new habitats

Alzate

Onstein

Etienne

et al. 2020

Oikos

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To successfully colonize new habitats, organisms not only need to gain access to it, they also need to cope with the selective pressures imposed by the local biotic and abiotic conditions. The number of immigrants, the preadaptation to the local habitat and the presence of competitors are important factors determining the success of colonization. Here, using two experimental set‐ups, we studied the effect of interspecific competition in combination with propagule pressure and preadaptation on the colonization success of new habitats. Our model system consisted of tomato plants (the novel habitat), the two‐spotted spider mite Tetranychus urticae as our focal species and the red spider mite Tetranychus evansi as a competitor. Our results show that propagule pressure and preadaptation positively affect colonization success. More successful populations reach larger final population sizes either by having higher per capita growth rates (due to preadaptation effects) or by starting a population with a larger number of individuals. Although populations are more successful colonizing non‐competitive environments than competitive ones, propagule pressure and preadaptation counteract the negative effects of competition, promoting colonization success. Our study shows the importance of propagule pressure and preadaptation for successful colonization of new habitats by providing the ability to cope with both the exigencies of new environments and the community context.

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Section: Discussionmentioning

confidence: 99%

The role of preadaptation, propagule pressure and competition in the colonization of new habitats

Alzate

Onstein

Etienne

et al. 2020

Oikos

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“…Although we certainly expect local adaptation of many populations (Antonovics 1987), we should not expect it to be temporally consistent if the environment is not (O'Brien et al 2017;Brady et al 2019). Although we certainly expect local adaptation of many populations (Antonovics 1987), we should not expect it to be temporally consistent if the environment is not (O'Brien et al 2017;Brady et al 2019).…”

Section: Plant-animal Interactionsmentioning

confidence: 94%

“…In year 2, there was no evidence for local adaptation of any population. Although we certainly expect local adaptation of many populations (Antonovics 1987), we should not expect it to be temporally consistent if the environment is not (O'Brien et al 2017;Brady et al 2019). Homing in on an optimal phenotype is made more difficult by temporal variation in selection (Milner et al 1999;Kirkpatrick and Peischl 2013;Hao et al 2015), and it is unlikely for a phenotype to arise anywhere that is optimally adapted to all possible conditions at that site across years.…”

Section: Plant-animal Interactionsmentioning

confidence: 99%

Maladaptation beyond a geographic range limit driven by antagonistic and mutualistic biotic interactions across an abiotic gradient

Benning

Moeller

2019

Evolution

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Species’ geographic range limits often result from maladaptation to the novel environments beyond the range margin. However, we rarely know which aspects of the n‐dimensional environment are driving this maladaptation. Especially of interest is the influence of abiotic versus biotic factors in delimiting species’ distributions. We conducted a 2‐year reciprocal transplant experiment involving manipulations of the biotic environment to explore how spatiotemporal gradients in precipitation, fatal mammalian herbivory, and pollination affected lifetime fitness within and beyond the range of the California annual plant, Clarkia xantiana ssp. xantiana. In the first, drier year of the experiment, fitness outside the range edge was limited mainly by low precipitation, and there was some evidence for local adaptation within the range. In the second, wetter year, we did not observe abiotic limitations to plant fitness outside the range; instead biotic interactions, especially herbivory, limited fitness outside the range. Together, protection from herbivory and supplementation of pollen resulted in three‐ to sevenfold increases in lifetime fitness outside the range margin in the abiotically benign year. Overall, our work demonstrates the importance of biotic interactions, particularly as they interact with the abiotic environment, in determining fitness beyond geographic range boundaries.

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“…Our experiment also pinpoints the consequences of such a hypermobility from an applied perspective [70]- [72]. Apart from the potential to impose maladaptation, or to hinder adaptation [73], [74], hypermobility is also able to lead to changes in the local and regional population dynamics, even to such a degree that local population extinction chances increase.…”

Section: Discussionmentioning

confidence: 74%

Individual heterogeneity and its importance for metapopulation dynamics

Masier

Dahirel

Mortier

et al. 2020

Preprint

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Habitat fragmentation reduces the area of habitat patches and their connectedness in the landscape. It is well established that the level of connectedness impacts connectivity and metapopulation dynamics, and is therefore a central tenet in conservation biology. Connectedness equally generates sorting of phenotypes within the spatial network and therefore impacts local and regional eco-evolutionary dynamics. Paradoxically, recommendations for species conservation rely on principles derived from theory that neglects any individual phenotypic heterogenety and spatial organization.By creating experimental metapopulations using the model species Tetranychus urticae (two-spotted spider mite) with three levels of landscape connectedness and by regularly removing phenotypic structure in a subset of these populations, we tested the degree to which regional and local population dynamics are determined both by network connectedness and the phenotypic spatial organization.Our results show that some aspects of metapopulation dynamics can be attributed to the evolution of dispersal. More importantly, we find self-organization of phenotypic spatial structure to equalize the effects of reduced connectedness on metapopulation dynamics. These changes were all in the direction of improved metapopulation persistence. Contrary to expectations, the most connected local patches showed an overall reduced local population size, possibly originating from a faster depletion of resources from immigrants or transiting individuals.This experiment shows how metapopulation dynamics can significantly deviate from theoretical expectations if individual heterogeneity is considered, and more importantly that disruption of this phenotypic self-structuring may drive metapopulation dynamics towards higher risks of extinction.Significance StatementChanges in connectedness impact metapopulation dynamics but also the spatial organization of individual phenotypic heterogeneity. The extent to which metapopulation dynamics depend on this phenotypic structuring is unknown, despite the fact metapopulation theory is at the heart of conservation biology. By using experimental metapopulations and a randomization treatment, we demonstrate that the emerging spatial organization of individuals (both genetically and phenotypically) is a major driver of metapopulation dynamics. This spatial organization may be important as it may equalize all variation in metapopulation dynamics across a gradient of connectivity. This potentially rescuing effect stemming from the self-organization of phenotypes in metapopulations is of uttermost importance for conservation and translocation actions.

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Understanding Maladaptation by Uniting Ecological and Evolutionary Perspectives

Cited by 65 publications

References 222 publications

The role of preadaptation, propagule pressure and competition in the colonization of new habitats

The role of preadaptation, propagule pressure and competition in the colonization of new habitats

Maladaptation beyond a geographic range limit driven by antagonistic and mutualistic biotic interactions across an abiotic gradient

Individual heterogeneity and its importance for metapopulation dynamics

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