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Neylan, I. P.

Publications and source records attributed to Neylan, I. P..

5 recordsLinked to original sources

Distinct molecular mechanisms shape thermal tolerance and its plasticity in a splash pool copepod

Understanding how organisms respond to changes in temperature is becoming increasingly important in our rapidly changing world. While species differ substantially in their thermal tolerance, the exact molecular mechanisms underpinning this trait variation remain largely unknown. Species with broad geographical distribution provide a unique opportunity to examine variable responses to temperature, as populations experience a diverse range of thermal regimes that differ in the intensity, frequency, and duration of thermal stress. We used a splash pool copepod (Tigriopus californicus) with a large geographic range across the North American coast (Baja California to Alaska) to examine variation in thermotolerance and the plasticity of thermotolerance in five populations sampled across 12 degrees of latitude. We found that populations with higher heat tolerance (southern) showed lower plasticity (measured as increased survival at higher temperatures after a prior exposure to sub-lethal temperature). Our comparative transcriptomic analyses revealed that higher heat tolerance was associated with maintaining elevated expression of genes coding for peptidases even in absence of heat shock and higher plasticity of heat tolerance was associated with an increase in gene expression plasticity of genes coding for chitin and extracellular matrix (ECM). Our results highlight ontology-specific patterns associated with changes in the trait means and plasticity of heat tolerance across populations. These findings improve our mechanistic knowledge of thermotolerance as a trait and our ability to predict which populations are most vulnerable to extinction based on the trade-off between fixed thermal limits and plastic responses.

evolutionary biology↗

The curious case of a Chilean copepod (Tigriopus aff. angulatus) genome assembly

Tigriopus copepods are found in splash pools on all seven continents from the equator to Arctic and Antarctic regions. Given their geographic distribution, frequent exposure to extreme environmental conditions, and strong signatures of local adaptation, these copepods have become models for exploring patterns of adaptation to stressful environments. However, most studies focus on a small subset of Tigriopus species, and there are few genome resources representing the diversity of Tigriopus species and populations. Here, we combine long-read, Pacific Biosciences HiFi data with short-read, Illumina HiC and RNA-seq data to assemble and annotate a genome representing a Tigriopus population from the coast of central Chile. Based on the level of divergence that we observed in mitochondrial genes, we also performed a comparison of morphological characteristics between this population and members of the T. angulatus complex. The assembly that we generated (qhTigAngs1.1.pri) includes 12 major scaffolds (N50 19Mbp, L50 7), equivalent to the number of chromosomes in other Tigriopus species. BUSCO and k-mer analyses of the assembly and BUSCO analyses of gene models are relatively complete (89-99%) with respect to gene or k-mer content. The level of divergence that we observed, morphological differences we recorded, and the spatial distance of this population from the type locality suggest that this Chilean population of Tigriopus may represent a novel species that we call Tigriopus aff. angulatus. These genomic resources will help us understand the diversity and structure of Tigriopus species and populations as well as facilitate future comparisons of adaptation across parallel environmental gradients.

genomics↗

Genetic assimilation and accommodation shape adaptation to heat stress in a splash pool copepod

Understanding how organisms respond to variable environments is becoming increasingly important in our rapidly changing world. Beyond genetic adaptation, plastic responses to the environment can alter phenotypes and fitness, ultimately driving evolution. However, the interaction between plasticity and adaptation during environmental change is complex and hard to measure in natural systems. Here, we used two populations of Tigriopus californicus copepods, a thermally tolerant southern population and a thermally sensitive northern population, to conduct a fully factorial split brood experiment where we exposed animals as larvae and adults to either a sublethal heat stress or control (no heat treatment) before measuring heat tolerance and gene expression patterns. We found that increased thermal tolerance across populations came at the expense of physiological plasticity and evolved through higher baseline expression of heat stress response genes across environmental contexts as well as increased gene expression plasticity in response to heat stress. In the thermally sensitive northern population, developmental exposure to heat stress led to higher adult tolerance and lower physiological plasticity underpinned by higher gene expression plasticity. Importantly, we found that the same set of genes were largely responsible for both the evolved higher tolerance in the southern population and the developmentally induced tolerance in the northern population suggesting that in this system, a shared molecular response contributes to acclimation and adaptation across both populations. These results link existing physiological plasticity with long-term evolutionary responses providing insight into how these populations will adapt and respond to future environmental change. SIGNIFICANCEUnderstanding plastic and evolutionary responses to dynamic environments is critical to anticipating species vulnerability to climate change. In this study, we compared gene expression and physiological responses to heat stress across two populations of a marine copepod that differ in thermal tolerance to investigate mechanisms of adaptation. We found evidence for plasticity-led evolution in this system, with the same set of genes contributing to long-term evolutionary changes across populations and to short-term physiological adjustments within populations. Our results suggest that populations with a reservoir of plasticity have a greater potential to evolve as the climate continues to warm, but that there may be a limit to this adaptive capacity.

evolutionary biology↗

Context matters: A meta-analysis of the variable impact of transgenerational and developmental plasticity on responses to stress

O_LIUnderstanding organisms abilities to adapt and acclimate to stressors in their environments is essential for predicting the distributions and persistence of species and populations during environmental change. Beyond genetic adaptation, prior experiences with a given stressor across life stages can dictate how an individual will fare when exposed to that stressor again. There is now a robust literature on the impacts of parental experiences on offspring traits (transgenerational plasticity), plus an even broader literature on the carry-over effects of early-life experience on phenotypic outcomes (within-generational or developmental plasticity); however, less is understood about the relative strengths of these two forms of plasticity and how they interact to shape stress tolerance. C_LIO_LIWe explored these questions by conducting a meta-analysis of peer-reviewed studies that tested both within- and transgenerational effects of naturally occurring environmental stressors. In particular, we explored contextual moderators or predictor variables including the traits measured, the type of stressor, taxonomic group, and organismal life history traits to elucidate patterns and develop a predictive framework for when we should expect to see effects of transgenerational plasticity, within-generational plasticity, both, or neither. C_LIO_LIWe found that there was not a strong or consistent directional effect of either parental or early-life exposure on subsequent offspring traits. Instead, experimental context (what stressor was used and what traits were measured) as well as biological context (taxonomy, life history traits) were important predictors for understanding the strength and direction of plasticity. We found several contexts where there were meaningful effects of parental and early-life stress exposure and where there was evidence that these may interact to impact phenotypic and fitness outcomes. C_LIO_LIOur study highlights the need for careful consideration of context when exploring patterns of plasticity. We hope to underscore the need for additional, fully factorial studies that measure the interaction between these forms of plasticity across a variety of systems and stressors to better understand how stress may carry forward across life stages and generations. C_LI

ecology↗

Evolutionary history mediates population response to rapid environmental change through within-generational and transgenerational plasticity

Rapid environmental change is affecting many organisms; some are coping well but many species are in decline. A key mechanism for facilitating success following environmental change is phenotypic plasticity. Organisms use cues to respond phenotypically to environmental conditions; many incorporate recent information (within-generation plasticity) and information from previous generations (transgenerational plasticity). We extend an existing evolutionary model where organisms utilize within-generational plasticity, transgenerational plasticity, rapid evolution, and bet-hedging. We show how, when rapid evolution of plasticity is not possible, the effect of environmental change (altering the environment mean, variance, or autocorrelation, or cue reliability) on population growth rate depends on selection for within-generation plasticity and transgenerational plasticity under historical environmental conditions. We then evaluate the predictions that populations adapted to highly variable environments, or with greater within-generational plasticity, are more likely to successfully respond to environmental change. We identify when these predictions fail, and show environmental change is most detrimental when previously reliable cues become unreliable. When multiple cues become unreliable, environmental change can cause deleterious effects regardless of the populations evolutionary history. Overall, this work provides a general framework for understanding the role of plasticity in population responses to rapid environmental change.

evolutionary biology↗