Negative relationship between thermal tolerance and plasticity in tolerance emerges during experimental evolution in a widespread marine invertebrate.
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ABSTRACT:
SUBMITTER: Sasaki MC
PROVIDER: S-EPMC8372069 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Sperm competition has classically been thought to maintain anisogamy (large eggs and smaller sperm) because males are thought to maximize their chance of winning fertilizations by trading sperm size for number. More recently it has been recognized that sperm quality (e.g., size, velocity) can also influence sperm competition, although studies have yielded conflicting results. Because sex evolved in the sea, debate has continued over the role of sperm competition and sperm environment in determining both sperm and egg size in externally fertilizing broadcast spawners. Remarkably, however, there have been no direct tests of whether broadcast spawners change the traits of their gametes depending on the likelihood of sperm competition. We manipulated the density (and thus, sperm environment) of a broadcast spawning ascidian (Styela plicata) in the field and then determined whether the phenotype of eggs and sperm changed. We found that sperm from adults kept at high density were larger and more motile than sperm from low-density adults. In vitro fertilizations revealed that sperm from high-density adults also lived longer and induced less polyspermy. Adult density also affected egg traits: eggs from high-density adults were smaller targets for sperm overall but produced larger ovicells than eggs from low-density adults. This suggests that broadcast spawning mothers balance (potentially conflicting) pre- and postzygotic selection pressures on egg size. Overall, our results suggest that sperm competition does not represent a strong force maintaining anisogamy in broadcast spawners. Instead, sperm limitation seems to select for large eggs and smaller, more numerous sperm.
| S-EPMC2533220 | biostudies-literature
Project description:BackgroundMany organisms are responding to climate change with dramatic range shifts, involving plastic and genetic changes to cope with novel climate regimes found at higher latitudes. Using experimental lineages of the seed beetle Callosobruchus maculatus, we simulated the initial phase of colonisation to progressively cooler and/or more variable conditions, to investigate how adaptation and phenotypic plasticity contribute to shifts in thermal tolerance during colonisation of novel climates.ResultsWe show that heat and cold tolerance rapidly evolve during the initial stages of adaptation to progressively cooler and more variable climates. The evolved shift in cold tolerance is, however, associated with maladaptive plasticity under the novel conditions, resulting in a pattern of countergradient variation between the ancestral and novel, fluctuating thermal environment. In contrast, lineages exposed to progressively cooler, but constant, temperatures over several generations expressed only beneficial plasticity in cold tolerances and no evolved response.ConclusionsWe propose that thermal adaptation during a range expansion to novel, more variable climates found at high latitudes and elevations may typically involve genetic compensation arising from maladaptive plasticity in the initial stages of adaptation, and that this form of (countergradient) thermal adaptation may represent an opportunity for more rapid and labile evolutionary change in thermal tolerances than via classic genetic assimilation models for thermal tolerance evolution (i.e., selection on existing reaction norms). Moreover, countergradient variation in thermal tolerances may typically mask cryptic genetic variability for these traits, resulting in apparent evolutionary stasis in thermal traits.
| S-EPMC7181507 | biostudies-literature
Project description:BACKGROUND:Colonial invertebrates such as corals exhibit nested levels of modularity, imposing a challenge to the depiction of their morphological evolution. Comparisons among diverse Caribbean gorgonian corals suggest decoupling of evolution at the polyp vs. branch/internode levels. Thus, evolutionary change in polyp form or size (the colonial module sensu stricto) does not imply a change in colony form (constructed of modular branches and other emergent features). This study examined the patterns of morphological integration at the intraspecific level. Pseudopterogorgia bipinnata (Verrill) (Octocorallia: Gorgoniidae) is a Caribbean shallow water gorgonian that can colonize most reef habitats (shallow/exposed vs. deep/protected; 1-45 m) and shows great morphological variation. RESULTS:To characterize the genotype/environment relationship and phenotypic plasticity in P. bipinnata, two microsatellite loci, mitochondrial (MSH1) and nuclear (ITS) DNA sequences, and (ITS2) DGGE banding patterns were initially compared among the populations present in the coral reefs of Belize (Carrie Bow Cay), Panama (Bocas del Toro), Colombia (Cartagena) and the Bahamas (San Salvador). Despite the large and discrete differentiation of morphotypes, there was no concordant genetic variation (DGGE banding patterns) in the ITS2 genotypes from Belize, Panama and Colombia. ITS1-5.8S-ITS2 phylogenetic analysis afforded evidence for considering the species P. kallos (Bielschowsky) as the shallow-most morphotype of P. bipinnata from exposed environments. The population from Carrie Bow Cay, Belize (1-45 m) was examined to determine the phenotypic integration of modular features such as branch thickness, polyp aperture, inter-polyp distance, internode length and branch length. Third-order partial correlation coefficients suggested significant integration between polypar and colonial traits. Some features did not change at all despite 10-fold differences in other integrated features. More importantly, some colonial features showed dependence on modular features. CONCLUSION:Consequently, module integration in gorgonian corals can be shifted, switched or canalized along lineages. Modular marine organisms such as corals are variations on a single theme: their modules can couple or decouple, allowing them to adapt to all marine benthic environments.
| S-EPMC1959521 | biostudies-literature
Project description:Complex life cycles characterized by uncertainty at transitions between larval/juvenile and adult environments could favour irreversible physiological plasticity at such transitions. To assess whether thermal tolerance of intertidal mussels (Mytilus californianus) adjusts to post-settlement environmental conditions, we collected juveniles from their thermally buffered microhabitat from high- and low-shore locations at cool (wave-exposed) and warm (wave-protected) sites. Juveniles were transplanted to unsheltered cages at the two low sites or placed in a common garden. Juveniles transplanted to the warm site for one month in summer had higher thermal tolerance, regardless of origin site. By contrast, common-garden juveniles from all sites had lower tolerance indistinguishable from exposed site transplants. After six months in the field plus a common garden period, there was a trend for higher thermal tolerance at the protected site, while reduced thermal tolerance at both sites indicated seasonal acclimatization. Thermal tolerance and growth rate were inversely related after one but not six months; protected-site transplants were more tolerant but grew more slowly. In contrast to juveniles, adults from low-shore exposed and protected sites retained differences in thermal tolerance after common garden treatment in summer. Both irreversible and reversible forms of plasticity must be considered in organismal responses to changing environments.
| S-EPMC5936721 | biostudies-literature
Project description:Pollen transport by water-flow (hydrophily) is a typical, and almost exclusive, adaptation of plants to life in the marine environment. It is thought that, unlike terrestrial environments, animals are not involved in pollination in the sea. The male flowers of the tropical marine angiosperm Thalassia testudinum open-up and release pollen in mucilage at night when invertebrate fauna is active. Here we present experimental evidence that, in the absence of water-flow, these invertebrates visit the flowers, carry and transfer mucilage mass with embedded pollen from the male flowers to the stigmas of the female flowers. Pollen tubes are formed on the stigmas, indicating that pollination is successful. Thus, T. testudinum has mixed abiotic-biotic pollination. We propose a zoobenthophilous pollination syndrome (pollen transfer in the benthic zone by invertebrate animals) which shares many characteristics with hydrophily, but flowers are expected to open-up during the night.
| S-EPMC5056424 | biostudies-literature
Project description:Microbial communities respond to temperature with physiological adaptation and compositional turnover. Whether thermal selection of enzymes explains marine microbiome plasticity in response to temperature remains unresolved. By quantifying the thermal behaviour of seven functionally-independent enzyme classes (esterase, extradiol dioxygenase, phosphatase, beta-galactosidase, nuclease, transaminase, and aldo-keto reductase) in native proteomes of marine sediment microbiomes from the Irish Sea to the southern Red Sea, we record a significant effect of the mean annual temperature (MAT) on enzyme response in all cases. Activity and stability profiles of 228 esterases and 5 extradiol dioxygenases from sediment and seawater across 70 locations worldwide validate this thermal pattern. Modelling the esterase phase transition temperature as a measure of structural flexibility confirms the observed relationship with MAT. Furthermore, when considering temperature variability in sites with non-significantly different MATs, the broadest range of enzyme thermal behaviour and the highest growth plasticity of the enriched heterotrophic bacteria occur in samples with the widest annual thermal variability. These results indicate that temperature-driven enzyme selection shapes microbiome thermal plasticity and that thermal variability finely tunes such processes and should be considered alongside MAT in forecasting microbial community thermal response.
| S-EPMC9958047 | biostudies-literature
Project description:BackgroundAnimal responses to thermal stimuli involve intricate contributions of genetics, neurobiology and physiology, with temperature variation providing a pervasive environmental factor for natural selection. Thermal behavior thus exemplifies a dynamic trait that requires non-trivial phenotypic summaries to appropriately capture the trait in response to a changing environment. To characterize the deterministic and plastic components of thermal responses, we developed a novel micro-droplet assay of nematode behavior that permits information-dense summaries of dynamic behavioral phenotypes as reaction norms in response to increasing temperature (thermal tolerance curves, TTC).ResultsWe found that C. elegans TTCs shift predictably with rearing conditions and developmental stage, with significant differences between distinct wildtype genetic backgrounds. Moreover, after screening TTCs for 58 C. elegans genetic mutant strains, we determined that genes affecting thermosensation, including cmk-1 and tax-4, potentially play important roles in the behavioral control of locomotion at high temperature, implicating neural decision-making in TTC shape rather than just generalized physiological limits. However, expression of the transient receptor potential ion channel TRPA-1 in the nervous system is not sufficient to rescue rearing-dependent plasticity in TTCs conferred by normal expression of this gene, indicating instead a role for intestinal signaling involving TRPA-1 in the adaptive plasticity of thermal performance.ConclusionsThese results implicate nervous system and non-nervous system contributions to behavior, in addition to basic cellular physiology, as key mediators of evolutionary responses to selection from temperature variation in nature.
| S-EPMC6558720 | biostudies-literature
Project description:In the face of global warming, both the absolute thermal tolerance of an ectotherm, and its ability to shift its tolerance level via acclimation, are thought to be fundamentally important. Understanding the links between tolerance and its plasticity is therefore critical to accurately predict vulnerability to warming. Previous studies in a number of ectotherm taxa suggest trade-offs in the evolution of thermal tolerance and its plasticity, something which does not, however, apply to Deronectes diving beetles, where these traits are instead positively correlated. Here we revisit the relationship between thermal tolerance and plasticity in these beetles, paying attention to a recently discovered morphological adaptation supporting under water respiration - setal tracheal gills. Hollow setae on the elytra interconnect with the beetle's tracheal system, providing a gas exchange surface that allows oxygen to be extracted directly from the water. This enables individuals to stay submerged for longer than their subelytral air stores would allow. We show that hypoxia reduced heat tolerance, especially when individuals were denied access to air, forcing them to rely solely on aquatic gas exchange. Species with higher densities of these gas-exchanging setae exhibited improved cold tolerance, but reduced heat tolerance and lower plasticity of heat tolerance. Differences in setal tracheal gill density across species were also related to habitat use: species with low gill density were found mainly in intermittent, warmer rivers, where underwater gas exchange is more problematic and risks of surfacing may be smaller. Moreover, when controlling for differences in gill density we no longer found a significant relationship between heat tolerance and its plasticity, suggesting that the previously reported positive relationship between these variables may be driven by differences in gill density. Differences in environmental conditions between the preferred habitats could simultaneously select for characteristic differences in both thermal tolerance and gill density. Such simultaneous selection may have resulted in a non-causal association between cold tolerance and gill density. For heat tolerance, the correlations with gill density could reflect a causal relationship. Species relying strongly on diffusive oxygen uptake via setal tracheal gills may have a reduced oxygen supply capacity and may be left with fewer options for matching oxygen uptake to oxygen demand during acclimation, which could explain their reduced heat tolerance and limited plasticity. Our study helps shed light on the mechanisms that underpin thermal tolerance and plasticity in diving air-breathing ectotherms, and explores how differences in thermal tolerance across species are linked to their selected habitat, morphological adaptations and evolutionary history.
| S-EPMC5968350 | biostudies-literature
Project description:The Mediterranean Sea is warming at three times the rate of the global ocean raising concerns about the vulnerability of marine organisms to climate change. Macrophytes play a key role in coastal ecosystems, therefore predicting how warming will affect these key species is critical to understand the effects of climate change on Mediterranean coastal ecosystems. We measured the physiological performance of six dominant native Mediterranean macrophytes under ten temperature treatments ranging from 12 to 34°C to examine their thermal niche, and vulnerability to projected warming in the western Mediterranean up until 2100. Among the macrophytes tested, Cymodocea nodosa was the species with the highest thermal optima and it was beyond current summer temperature. Therefore, C. nodosa may benefit from projected warming over the coming century. The optimal temperature for growth of the other species (Posidonia oceanica, Cystoseira compressa, Padina pavonica, Caulerpa prolifera, and Halimeda tuna) was lower. Similarly, the species presented different upper lethal limits, spanning at least across 5.1°C between 28.9°C (P. oceanica) and >34°C (C. nodosa). Our results demonstrate the variable physiological responses of species within the same local community to temperature changes and highlight important potential differences in climate change vulnerability, among species within coastal marine ecosystems.
| S-EPMC6303755 | biostudies-literature
Project description:Understanding the factors affecting thermal tolerance is crucial for predicting the impact climate change will have on ectotherms. However, the role developmental plasticity plays in allowing populations to cope with thermal extremes is poorly understood. Here, we meta-analyse how thermal tolerance is initially and persistently impacted by early (embryonic and juvenile) thermal environments by using data from 150 experimental studies on 138 ectothermic species. Thermal tolerance only increased by 0.13°C per 1°C change in developmental temperature and substantial variation in plasticity (~36%) was the result of shared evolutionary history and species ecology. Aquatic ectotherms were more than three times as plastic as terrestrial ectotherms. Notably, embryos expressed weaker but more heterogenous plasticity than older life stages, with numerous responses appearing as non-adaptive. While developmental temperatures did not have persistent effects on thermal tolerance overall, persistent effects were vastly under-studied, and their direction and magnitude varied with ontogeny. Embryonic stages may represent a critical window of vulnerability to changing environments and we urge researchers to consider early life stages when assessing the climate vulnerability of ectotherms. Overall, our synthesis suggests that developmental changes in thermal tolerance rarely reach levels of perfect compensation and may provide limited benefit in changing environments.
| S-EPMC9804923 | biostudies-literature