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Behaviour, life history and persistence in novel environments.

ABSTRACT: Understanding what affects population growth in novel environments is fundamental to forecast organisms' responses to global change, including biological invasions and land use intensification. Novel environments are challenging because they can cause maladaptation, increasing the risk of extinction by negative population growth. Animals can avoid extinction by improving the phenotype-environment match through behavioural responses, notably matching habitat choice and learning. However, the demographic consequences of these responses remain insufficiently understood in part because they have not been analysed within a life-history context. By means of an individual-based model, we show here that matching habitat choice and learning interact with life history to influence persistence in novel environments. In maladaptive contexts, the likelihood of persisting is higher for life-history strategies that increase the value of adults over the value of offspring, even at the cost of decreasing reproduction. Such a strategy facilitates persistence in novel environments by reducing the costs of a reproductive failure while increasing the benefits of behavioural responses. Our results reinforce the view that a more predictive theory for extinction risk under rapid environmental changes requires considering behavioural responses and life history as part of a common adaptive strategy to cope with environmental changes. This article is part of the theme issue 'Linking behaviour to dynamics of populations and communities: application of novel approaches in behavioural ecology to conservation'.

SUBMITTER: Maspons J

PROVIDER: S-EPMC6710578 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Temporal variation in demographic processes can greatly impact population dynamics. Perturbations of statistical coefficients that describe demographic rates within matrix models have, for example, revealed that stochastic population growth rates (log(λ s)) of fast life histories are more sensitive to temporal autocorrelation of environmental conditions than those of slow life histories. Yet, we know little about the mechanisms that drive such patterns. Here, we used a mechanistic, functional trait approach to examine the functional pathways by which a typical fast life history species, the macrodetrivore Orchestia gammarellus, and a typical slow life history species, the reef manta ray Manta alfredi, differ in their sensitivity to environmental autocorrelation if (a) growth and reproduction are described mechanistically by functional traits that adhere to the principle of energy conservation, and if (b) demographic variation is determined by temporal autocorrelation in food conditions. Opposite to previous findings, we found that O. gammarellus log(λ s) was most sensitive to the frequency of good food conditions, likely because reproduction traits, which directly impact population growth, were most influential to log(λ s). Manta alfredi log(λs ) was instead most sensitive to temporal autocorrelation, likely because growth parameters, which impact population growth indirectly, were most influential to log(λ s). This differential sensitivity to functional traits likely also explains why we found that O. gammarellus mean body size decreased (due to increased reproduction) but M. alfredi mean body size increased (due to increased individual growth) as food conditions became more favorable. Increasing demographic stochasticity under constant food conditions decreased O. gammarellus mean body size and increased log(λ s) due to increased reproduction, whereas M. alfredi mean body and log(λ s) decreased, likely due to decreased individual growth. Our findings signify the importance of integrating functional traits into demographic models as this provides mechanistic understanding of how environmental and demographic stochasticity affects population dynamics in stochastic environments.

Project description:BackgroundOrganisms live in environments that vary. For life-history traits that vary across environments, fitness will be maximised when the phenotype is appropriately matched to the environmental conditions. For the free-living nematode Caenorhabditis elegans, we have investigated how two major life-history traits, (i) the development of environmentally resistant dauer larvae and (ii) reproduction, respond to environmental stress (high population density and low food availability), and how these traits vary between lines and the genetic basis of this variation.ResultsWe found that lines of C. elegans vary in their phenotypic plasticity of dauer larva development, i.e. there is variation in the likelihood of developing into a dauer larva for the same environmental change. There was also variation in how lifetime fecundity and the rate of reproduction changed under conditions of environmental stress. These traits were related, such that lines that are highly plastic for dauer larva development also maintain a high population growth rate when stressed. We identified quantitative trait loci (QTL) on two chromosomes that control the dauer larva development and population size phenotypes. The QTLs affecting the dauer larva development and population size phenotypes on chromosome II are closely linked, but are genetically separable. This chromosome II QTL controlling dauer larva development does not encompass any loci previously identified to control dauer larva development. This chromosome II region contains many predicted 7-transmembrane receptors. Such proteins are often involved in information transduction, which is clearly relevant to the control of dauer larva development.ConclusionC. elegans alters both its larval development and adult reproductive strategy in response to environmental stress. Together the phenotypic and genotypic data suggest that these two major life-history traits are co-ordinated responses to environmental stress and that they are, at least in part, controlled by the same genomic regions.

Project description:BackgroundUncovering the mechanisms underlying rapid genetic adaptation can provide insight into adaptive evolution and shed light on conservation, invasive species control, and natural resource management. However, it can be difficult to experimentally explore rapid adaptation due to the challenges associated with propagating and maintaining species in captive environments for long periods of time. By contrast, many introduced species have experienced strong selection when colonizing environments that differ substantially from their native range and thus provide a "natural experiment" for studying rapid genetic adaptation. One such example occurred when sea lamprey (Petromyzon marinus), native to the northern Atlantic, naturally migrated into Lake Champlain and expanded their range into the Great Lakes via man-made shipping canals.ResultsUtilizing 368,886 genome-wide single nucleotide polymorphisms (SNPs), we calculated genome-wide levels of genetic diversity (i.e., heterozygosity and π) for sea lamprey collected from native (Connecticut River), native but recently colonized (Lake Champlain), and invasive (Lake Michigan) populations, assessed genetic differentiation between all populations, and identified candidate genes that responded to selection imposed by the novel environments. We observed a 14 and 24% reduction in genetic diversity in Lake Michigan and Lake Champlain populations, respectively, compared to individuals from the Connecticut River, suggesting that sea lamprey populations underwent a genetic bottleneck during colonization. Additionally, we identified 121 and 43 outlier genes in comparisons between Lake Michigan and Connecticut River and between Lake Champlain and Connecticut River, respectively. Six outlier genes that contained synonymous SNPs in their coding regions and two genes that contained nonsynonymous SNPs may underlie the rapid evolution of growth (i.e., GHR), reproduction (i.e., PGR, TTC25, STARD10), and bioenergetics (i.e., OXCT1, PYGL, DIN4, SLC25A15).ConclusionsBy identifying the genomic basis of rapid adaptation to novel environments, we demonstrate that populations of invasive species can be a useful study system for understanding adaptive evolution. Furthermore, the reduction in genome-wide levels of genetic diversity associated with colonization coupled with the identification of outlier genes underlying key life history traits known to have changed in invasive sea lamprey populations (e.g., growth, reproduction) illustrate the utility in applying genomic approaches for the successful management of introduced species.

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Behaviour, life history and persistence in novel environments.

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