The value of space‐for‐time substitution for studying fine‐scale microevolutionary processes

Wogan, Guinevere O. U.; Wang, Ian

doi:10.1111/ecog.03235

Cited by 54 publications

(42 citation statements)

References 108 publications

(160 reference statements)

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“…When the cost is high and genetic tracking of the environment is easy, the plastic slope tends to zero; but when the cost is low and genetic tracking hard, the slope tends to the regression of the optimum on the environment of development (DO-regression) (Gavrilets and Scheiner 1993). The plastic slope that evolves is symmetric with respect to temporal and spatial parameters, providing a theoretical basis for the assumptions underlying space-for-time substitutions in empirical work (Wogan and Wang 2017). However, temporal and spatial fluctuations can have asymmetric influences if there are differences in the values of their homologous parameters, suggesting care must be taken.…”

Section: Discussionmentioning

confidence: 99%

The evolution of phenotypic plasticity when environments fluctuate in time and space

King

Hadfield

2019

Evolution Letters

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Most theoretical studies have explored the evolution of plasticity when the environment, and therefore the optimal trait value, varies in time or space. When the environment varies in time and space, we show that genetic adaptation to Markovian temporal fluctuations depends on the between‐generation autocorrelation in the environment in exactly the same way that genetic adaptation to spatial fluctuations depends on the probability of philopatry. This is because both measure the correlation in parent‐offspring environments and therefore the effectiveness of a genetic response to selection. If the capacity to genetically respond to selection is stronger in one dimension (e.g., space), then plasticity mainly evolves in response to fluctuations in the other dimension (e.g., time). If the relationships between the environments of development and selection are the same in time and space, the evolved plastic response to temporal fluctuations is useful in a spatial context and genetic differentiation in space is reduced. However, if the relationships between the environments of development and selection are different, the optimal level of plasticity is different in the two dimensions. In this case, the plastic response that evolves to cope with temporal fluctuations may actually be maladaptive in space, resulting in the evolution of hyperplasticity or negative plasticity. These effects can be mitigated by spatial genetic differentiation that acts in opposition to plasticity resulting in counter‐gradient variation. These results highlight the difficulty of making space‐for‐time substitutions in empirical work but identify the key parameters that need to be measured in order to test whether space‐for‐time substitutions are likely to be valid.

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Section: Discussionmentioning

confidence: 99%

The evolution of phenotypic plasticity when environments fluctuate in time and space

King

Hadfield

2019

Evolution Letters

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“…Here, we reconstructed patterns of genome‐wide diversity and investigated evidence for local adaption by identifying genotype‐environment associations across two independent elevational transects of American pika populations. We employed RADseq genotyping‐by‐sequencing within a space‐for‐time design, which enabled us to circumvent the difficulties associated with long‐term genetic monitoring and allowed us to highlight several environmental axes potentially driving natural selection (Lotterhos & Whitlock, ; Wogan & Wang, ). Additionally, GEA methods have relatively high power to resolve loci under natural selection (De Mita et al., ), and do not require specific candidate loci (Hoffmann & Willi, ).…”

Section: Discussionmentioning

confidence: 99%

“…GEA methods seek to detect natural selection by scanning for meaningful associations between allele frequencies and environmental pressures. Such methods can be effectively applied over elevational gradients, so that contemporary spatial patterns across rapidly changing environments can be used to reflect changes through time (i.e., space‐for‐time design; reviewed in Wogan & Wang, ). For example, Guo, Lu, Liao, and Merilä () found climate‐associated adaptive divergence in genes associated with binding and metabolic processes in elevationally distributed populations of Andrew's toads ( Bufo andrewsi ) after controlling for neutral divergence.…”

Section: Introductionmentioning

confidence: 99%

Adaptive population divergence and directional gene flow across steep elevational gradients in a climate‐sensitive mammal

et al. 2018

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The ecological effects of climate change have been shown in most major taxonomic groups; however, the evolutionary consequences are less well-documented. Adaptation to new climatic conditions offers a potential long-term mechanism for species to maintain viability in rapidly changing environments, but mammalian examples remain scarce. The American pika (Ochotona princeps) has been impacted by recent climate-associated extirpations and range-wide reductions in population sizes, establishing it as a sentinel mammalian species for climate change. To investigate evidence for local adaptation and reconstruct patterns of genomic diversity and gene flow across rapidly changing environments, we used a space-for-time design and restriction site-associated DNA sequencing to genotype American pikas along two steep elevational gradients at 30,966 SNPs and employed independent outlier detection methods that scanned for genotype-environment associations. We identified 338 outlier SNPs detected by two separate analyses and/or replicated in both transects, several of which were annotated to genes involved in metabolic function and oxygen transport. Additionally, we found evidence of directional gene flow primarily downslope from high-elevation populations, along with reduced gene flow at outlier loci. If this trend continues, elevational range contractions in American pikas will likely be from local extirpation rather than upward movement of low-elevation individuals; this, in turn, could limit the potential for adaptation within this landscape. These findings are of particular relevance for future conservation and management of American pikas and other elevationally restricted, thermally sensitive species.

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“…In such case, the performance of the low‐latitude populations at their current higher environmental temperature can then be used as a proxy for the performance of the high‐latitude populations when they gradually evolve (hence genetically adapt) under future warming (De Frenne et al., ). While this approach should be done cautiously as time‐scales differ and it assumes that the drivers of trait change in space are the same as those that drive trait change through time, this approach has been shown reliable to infer micro‐evolutionary processes (Wogan & Wang, ).…”

Section: Introductionmentioning

confidence: 99%

Temperature variation makes an ectotherm more sensitive to global warming unless thermal evolution occurs

Verheyen

Stoks

2019

Journal of Animal Ecology

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1. To assess long-term impacts of global warming on species, there is growing interest in latitudinal intraspecific patterns in thermal adaptation. Yet, while both mean temperatures and daily temperature fluctuations (DTFs) are expected to increase under global warming, latitudinal differences in the effects of DTFs have not been documented.2. We tested whether low-latitude populations of an ectotherm deal better with greater DTF than high-latitude populations, especially at a high mean temperature close to the optimal temperature for growth where DTF causes exposure to extreme high temperatures. We evaluated the impact of DTFs when assessing the effect of gradual thermal evolution at the high latitude with a space-for-time substitution.3. We compared effects of both mean temperatures (20 and 24°C) and DTFs (constant = 0°C, low = 5°C and high = 10°C) on growth rates between low-latitude and high-latitude populations of the damselfly Ischnura elegans in a commongarden experiment. 4. DTFs, if anything, reduced growth and were generally stressful as indicated by reductions in body condition, antioxidant defence and metabolic rate, and increases in oxidative damage. Most negative effects of DTFs were only present at a mean of 24°C when too high temperatures were reached during a daily cycle.Notably, while 4°C warming was beneficial in terms of growth rate at both latitudes at a constant temperature regime, this changed in a negative effect at high DTF. Moreover, this modulating effect of the mean temperature by DTF differed between latitudes indicating local thermal adaptation. While 4°C warming at low DTF still caused faster growth in low-latitude larvae, it already slowed growth in high-latitude larvae. This supports the emerging insight that warming would increase growth in high-latitude larvae in the absence of DTF, yet would decrease growth in the more realistic scenarios with DTF. In contrast, a space-for-time substitution approach suggested that under gradual thermal evolution, the evolved high-latitude larvae would no longer suffer a growth reduction in the presence of DTF. 5.Our study provided important proof-of-principle that jointly integrating gradual thermal evolution and the expected increase in DTF generates opposing predictions of effects of global warming on this ectotherm. Additional supporting information may be found online in the Supporting Information section at the end of the article.How to cite this article: Verheyen J, Stoks R. Temperature variation makes an ectotherm more sensitive to global warming unless thermal evolution occurs. J Anim Ecol.

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The value of space‐for‐time substitution for studying fine‐scale microevolutionary processes

Cited by 54 publications

References 108 publications

The evolution of phenotypic plasticity when environments fluctuate in time and space

The evolution of phenotypic plasticity when environments fluctuate in time and space

Adaptive population divergence and directional gene flow across steep elevational gradients in a climate‐sensitive mammal

Temperature variation makes an ectotherm more sensitive to global warming unless thermal evolution occurs

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