Probabilistic measures for biological adaptation and resilience.

This paper introduces an approach to quantifying ecological resilience in biological systems, particularly focusing on noisy systems responding to episodic disturbances with sudden adaptations. Incorporating concepts from nonequilibrium statistical mechanics, we propose a measure termed "ecological resilience through adaptation," specifically tailored to noisy, forced systems that undergo physiological adaptation in the face of stressful environmental changes. Randomness plays a key role, accounting for model uncertainty and the inherent variability in the dynamical response among components of biological systems. Our measure of resilience is rooted in the probabilistic description of states within these systems and is defined in terms of the dynamics of the ensemble average of a model-specific observable quantifying success or well-being. Our approach utilizes stochastic linear response theory to compute how the expected success of a system, originally in statistical equilibrium, dynamically changes in response to a environmental perturbation and a subsequent adaptation. The resulting mathematical derivations allow for the estimation of resilience in terms of ensemble averages of simulated or experimental data. Finally, through a simple but clear conceptual example, we illustrate how our resilience measure can be interpreted and compared to other existing frameworks in the literature. The methodology is general but inspired by applications in plant systems, with the potential for broader application to complex biological processes.

Design Principles for Biological Adaptation: A Systems and Control-Theoretic Treatment.

Establishing a mapping between (from and to) the functionality of interest and the underlying network structure (design principles) remains a crucial step toward understanding and design of bio-systems. Perfect adaptation is one such crucial functionality that enables every living organism to regulate its essential activities in the presence of external disturbances. Previous approaches to deducing the design principles for adaptation have either relied on computationally burdensome brute-force methods or rule-based design strategies detecting only a subset of all possible adaptive network structures. This chapter outlines a scalable and generalizable method inspired by systems theory that unravels an exhaustive set of adaptation-capable structures. We first use the well-known performance parameters to characterize perfect adaptation. These performance parameters are then mapped back to a few parameters (poles, zeros, gain) characteristic of the underlying dynamical system constituted by the rate equations. Therefore, the performance parameters evaluated for the scenario of perfect adaptation can be expressed as a set of precise mathematical conditions involving the system parameters. Finally, we use algebraic graph theory to translate these abstract mathematical conditions to certain structural requirements for adaptation. The proposed algorithm does not assume any particular dynamics and is applicable to networks of any size. Moreover, the results offer a significant advancement in the realm of understanding and designing complex biochemical networks.

Linking morphology, performance, and habitat utilization: adaptation across biologically relevant 'levels' in tamarins.

BACKGROUND: Biological adaptation manifests itself at the interface of different biologically relevant 'levels', such as ecology, performance, and morphology. Integrated studies at this interface are scarce due to practical difficulties in study design. We present a multilevel analysis, in which we combine evidence from habitat utilization, leaping performance and limb bone morphology of four species of tamarins to elucidate correlations between these 'levels'. RESULTS: We conducted studies of leaping behavior in the field and in a naturalistic park and found significant differences in support use and leaping performance. Leontocebus nigrifrons leaps primarily on vertical, inflexible supports, with vertical body postures, and covers greater leaping distances on average. In contrast, Saguinus midas and S. imperator use vertical and horizontal supports for leaping with a relatively similar frequency. S. mystax is similar to S. midas and S. imperator in the use of supports, but covers greater leaping distances on average, which are nevertheless shorter than those of L. nigrifrons. We assumed these differences to be reflected in the locomotor morphology, too, and compared various morphological features of the long bones of the limbs. According to our performance and habitat utilization data, we expected the long bone morphology of L. nigrifrons to reflect the largest potential for joint torque generation and stress resistance, because we assume longer leaps on vertical supports to exert larger forces on the bones. For S. mystax, based on our performance data, we expected the potential for torque generation to be intermediate between L. nigrifrons and the other two Saguinus species. Surprisingly, we found S. midas and S. imperator having relatively more robust morphological structures as well as relatively larger muscle in-levers, and thus appearing better adapted to the stresses involved in leaping than the other two. CONCLUSION: This study demonstrates the complex ways in which behavioral and morphological 'levels' map onto each other, cautioning against oversimplification of ecological profiles when using large interspecific eco-morphological studies to make adaptive evolutionary inferences.

Dynamic Phytomeric Growth Contributes to Local Adaptation in Barley.

Vascular plants have segmented body axes with iterative nodes and internodes. Appropriate node initiation and internode elongation are fundamental to plant fitness and crop yield; however, how these events are spatiotemporally coordinated remains elusive. We show that in barley (Hordeum vulgare L.), selections during domestication have extended the apical meristematic phase to promote node initiation, but constrained subsequent internode elongation. In both vegetative and reproductive phases, internode elongation displays a dynamic proximal-distal gradient, and among subpopulations of domesticated barleys worldwide, node initiation and proximal internode elongation are associated with latitudinal and longitudinal gradients, respectively. Genetic and functional analyses suggest that, in addition to their converging roles in node initiation, flowering-time genes have been repurposed to specify the timing and duration of internode elongation. Our study provides an integrated view of barley node initiation and internode elongation and suggests that plant architecture should be recognized as a collection of dynamic phytomeric units in the context of crop adaptive evolution.

Convergence in carnivorous pitcher plants reveals a mechanism for composite trait evolution.

Composite traits involve multiple components that, only when combined, gain a new synergistic function. Thus, how they evolve remains a puzzle. We combined field experiments, microscopy, chemical analyses, and laser Doppler vibrometry with comparative phylogenetic analyses to show that two carnivorous Nepenthes pitcher plant species independently evolved similar adaptations in three distinct traits to acquire a new, composite trapping mechanism. Comparative analyses suggest that this new trait arose convergently through "spontaneous coincidence" of the required trait combination, rather than directional selection in the component traits. Our results indicate a plausible mechanism for composite trait evolution and highlight the importance of stochastic phenotypic variation as a facilitator of evolutionary novelty.

Frequent, infinitesimal bottlenecks maximize the rate of microbial adaptation.

Serial passaging is a fundamental technique in experimental evolution. The choice of bottleneck severity and frequency poses a dilemma: longer growth periods allow beneficial mutants to arise and grow over more generations, but simultaneously necessitate more severe bottlenecks with a higher risk of those same mutations being lost. Short growth periods require less severe bottlenecks, but come at the cost of less time between transfers for beneficial mutations to establish. The standard laboratory protocol of 24-h growth cycles with severe bottlenecking has logistical advantages for the experimenter but limited theoretical justification. Here we demonstrate that contrary to standard practice, the rate of adaptive evolution is maximized when bottlenecks are frequent and small, indeed infinitesimally so in the limit of continuous culture. This result derives from revising key assumptions underpinning previous theoretical work, notably changing the metric of optimization from adaptation per serial transfer to per experiment runtime. We also show that adding resource constraints and clonal interference to the model leaves the qualitative results unchanged. Implementing these findings will require liquid-handling robots to perform frequent bottlenecks, or chemostats for continuous culture. Further innovation in and adoption of these technologies has the potential to accelerate the rate of discovery in experimental evolution.

Ancient DNA genomics and the renaissance of herbaria.

Herbaria are undergoing a renaissance as valuable sources of genomic data for exploring plant evolution, ecology, and diversity. Ancient DNA retrieved from herbarium specimens can provide unprecedented glimpses into past plant communities, their interactions with biotic and abiotic factors, and the genetic changes that have occurred over time. Here, we highlight recent advances in the field of herbarium genomics and discuss the challenges and opportunities of combining data from modern and time-stamped historical specimens. We also describe how integrating herbarium genomics data with other data types can yield substantial insights into the evolutionary and ecological processes that shape plant communities. Herbarium genomic analysis is a tool for understanding plant life and informing conservation efforts in the face of dire environmental challenges.

Cycles of fusion and fission enabled rapid parallel adaptive radiations in African cichlids.

Although some lineages of animals and plants have made impressive adaptive radiations when provided with ecological opportunity, the propensities to radiate vary profoundly among lineages for unknown reasons. In Africa's Lake Victoria region, one cichlid lineage radiated in every lake, with the largest radiation taking place in a lake less than 16,000 years old. We show that all of its ecological guilds evolved in situ. Cycles of lineage fusion through admixture and lineage fission through speciation characterize the history of the radiation. It was jump-started when several swamp-dwelling refugial populations, each of which were of older hybrid descent, met in the newly forming lake, where they fused into a single population, resuspending old admixture variation. Each population contributed a different set of ancient alleles from which a new adaptive radiation assembled in record time, involving additional fusion-fission cycles. We argue that repeated fusion-fission cycles in the history of a lineage make adaptive radiation fast and predictable.

Community-wide genome sequencing reveals 30 years of Darwin's finch evolution.

A fundamental goal in evolutionary biology is to understand the genetic architecture of adaptive traits. Using whole-genome data of 3955 of Darwin's finches on the Galápagos Island of Daphne Major, we identified six loci of large effect that explain 45% of the variation in the highly heritable beak size of Geospiza fortis, a key ecological trait. The major locus is a supergene comprising four genes. Abrupt changes in allele frequencies at the loci accompanied a strong change in beak size caused by natural selection during a drought. A gradual change in Geospiza scandens occurred across 30 years as a result of introgressive hybridization with G. fortis. This study shows how a few loci with large effect on a fitness-related trait contribute to the genetic potential for rapid adaptive radiation.

Climate change adaptation needs a science of culture.

There is global consensus that we must immediately prioritize climate change adaptation-change in response to or anticipation of risks from climate change. Some researchers and policymakers urge 'transformative change', a complete break from past practices, yet report having little data on whether new practices reduce the risks communities face, even over the short term. However, researchers have some leads: human communities have long generated solutions to changing climate, and scientists who study culture have examples of effective and persistent solutions. This theme issue discusses cultural adaptation to climate change, and in this paper, we review how processes of biological adaptation, including innovation, modification, selective retention and transmission, shape the landscapes decision-makers care about-from which solutions emerge in communities, to the spread of effective adaptations, to regional or global collective action. We introduce a comprehensive portal of data and models on cultural adaptation to climate change, and we outline ways forward. This article is part of the theme issue 'Climate change adaptation needs a science of culture'.

Predicting the future.

Experiments on worms suggest that a statistical measure called the G matrix can accurately predict how phenotypes will adapt to a novel environment over multiple generations.

Transposable Elements: Epigenetic Silencing Mechanisms or Modulating Tools for Vertebrate Adaptations? Two Sides of the Same Coin.

Transposable elements constitute one of the main components of eukaryotic genomes. In vertebrates, they differ in content, typology, and family diversity and played a crucial role in the evolution of this taxon. However, due to their transposition ability, TEs can be responsible for genome instability, and thus silencing mechanisms were evolved to allow the coexistence between TEs and eukaryotic host-coding genes. Several papers are highlighting in TEs the presence of regulatory elements involved in regulating nearby genes in a tissue-specific fashion. This suggests that TEs are not sequences merely to silence; rather, they can be domesticated for the regulation of host-coding gene expression, permitting species adaptation and resilience as well as ensuring human health. This review presents the main silencing mechanisms acting in vertebrates and the importance of exploiting these mechanisms for TE control to rewire gene expression networks, challenging the general view of TEs as threatening elements.

North African fox genomes show signatures of repeated introgression and adaptation to life in deserts.

Elucidating the evolutionary process of animal adaptation to deserts is key to understanding adaptive responses to climate change. Here we generated 82 individual whole genomes of four fox species (genus Vulpes) inhabiting the Sahara Desert at different evolutionary times. We show that adaptation of new colonizing species to a hot arid environment has probably been facilitated by introgression and trans-species polymorphisms shared with older desert resident species, including a putatively adaptive 25 Mb genomic region. Scans for signatures of selection implicated genes affecting temperature perception, non-renal water loss and heat production in the recent adaptation of North African red foxes (Vulpes vulpes), after divergence from Eurasian populations approximately 78 thousand years ago. In the extreme desert specialists, Rueppell's fox (V. rueppellii) and fennec (V. zerda), we identified repeated signatures of selection in genes affecting renal water homeostasis supported by gene expression and physiological differences. Our study provides insights into the mechanisms and genetic underpinnings of a natural experiment of repeated adaptation to extreme conditions.

Extensive genetic admixture between Tai-Kadai-speaking people and their neighbours in the northeastern region of the Yungui Plateau inferred from genome-wide variations.

BACKGROUND: Yungui Plateau in Southwest China is characterized by multi-language and multi-ethnic communities and is one of the regions with the wealthiest ethnolinguistic, cultural and genetic diversity in East Asia. There are numerous Tai-Kadai (TK)-speaking populations, but their detailed evolutionary history and biological adaptations are still unclear. RESULTS: Here, we genotyped genome-wide SNP data of 77 unrelated TK-speaking Zhuang and Dong individuals from the Yungui Plateau and explored their detailed admixture history and adaptive features using clustering patterns, allele frequency differentiation and sharing haplotype patterns. TK-speaking Zhuang and Dong people in Guizhou are closely related to geographically close TK and Hmong-Mien (HM)-speaking populations. Besides, we identified that Guizhou TK-speaking people have a close genetic relationship with Austronesian (AN)-speaking Atayal and Paiwan people, which is supported by the common origin of the ancient Baiyue tribe. We additionally found subtle genetic differences among the newly studied TK people and previously reported Dais via the fine-scale genetic substructure analysis based on the shared haplotype chunks. Finally, we identified specific selection candidate signatures associated with several essential human immune systems and neurological disorders, which could provide evolutionary evidence for the allele frequency distribution pattern of genetic risk loci. CONCLUSIONS: Our comprehensive genetic characterization of TK people suggested the strong genetic affinity within TK groups and extensive gene flow with geographically close HM and Han people. We also provided genetic evidence that supported the common origin hypothesis of TK and AN people. The best-fitted admixture models further suggested that ancestral sources from northern millet farmers and southern inland and coastal people contributed to the formation of the gene pool of the Zhuang and Dong people.

Anthropogenic hybridization and its influence on the adaptive potential of the Sardinian wild boar (Sus scrofa meridionalis).

The wild boar (Sus scrofa meridionalis) arrived in Sardinia with the first human settlers in the early Neolithic with the potential to hybridize with the domestic pig (S. s. domesticus) throughout its evolution on the island. In this paper, we investigated the possible microevolutionary effects of such introgressive hybridization on the present wild boar population, comparing Sardinian wild specimens with several commercial pig breeds and Sardinian local pigs, along with a putatively unadmixed wild boar population from Central Italy, all genotyped with a medium density SNP chip. We first aimed at identifying hybrids in the population using different approaches, then examined genomic regions enriched for domestic alleles in the hybrid group, and finally we applied two methods to find regions under positive selection to possibly highlight instances of domestic adaptive introgression into a wild population. We found three hybrids within the Sardinian sample (3.1% out of the whole dataset). We reported 11 significant windows under positive selection with a method that looks for overly differentiated loci in the target population, compared with other two populations. We also identified 82 genomic regions with signs of selection in the domestic pig but not in the wild boar, two of which overlapped with genomic regions enriched for domestic alleles in the hybrid pool. Genes in these regions can be linked with reproductive success. Given our results, domestic introgression does not seem to be pervasive in the Sardinian wild boar. Nevertheless, we suggest monitoring the possible spread of advantageous domestic alleles in the coming years.

Adaptation of a quantitative trait to a changing environment: New analytical insights on the asexual and infinitesimal sexual models.

Predicting the adaptation of populations to a changing environment is crucial to assess the impact of human activities on biodiversity. Many theoretical studies have tackled this issue by modeling the evolution of quantitative traits subject to stabilizing selection around an optimal phenotype, whose value is shifted continuously through time. In this context, the population fate results from the equilibrium distribution of the trait, relative to the moving optimum. Such a distribution may vary with the shape of selection, the system of reproduction, the number of loci, the mutation kernel or their interactions. Here, we develop a methodology that provides quantitative measures of population maladaptation and potential of survival directly from the entire profile of the phenotypic distribution, without any a priori on its shape. We investigate two different systems of reproduction (asexual and infinitesimal sexual models of inheritance), with various forms of selection. In particular, we recover that fitness functions such that selection weakens away from the optimum lead to evolutionary tipping points, with an abrupt collapse of the population when the speed of environmental change is too high. Our unified framework allows deciphering the mechanisms that lead to this phenomenon. More generally, it allows discussing similarities and discrepancies between the two systems of reproduction, which are ultimately explained by different constraints on the evolution of the phenotypic variance. We demonstrate that the mean fitness in the population crucially depends on the shape of the selection function in the infinitesimal sexual model, in contrast with the asexual model. In the asexual model, we also investigate the effect of the mutation kernel and we show that kernels with higher kurtosis tend to reduce maladaptation and improve fitness, especially in fast changing environments.

The evolution of fast-growing coral reef fishes.

Individual growth is a fundamental life history trait1-4, yet its macroevolutionary trajectories have rarely been investigated for entire animal assemblages. Here we analyse the evolution of growth in a highly diverse vertebrate assemblage-coral reef fishes. We combine state-of-the-art extreme gradient boosted regression trees with phylogenetic comparative methods to detect the timing, number, location and magnitude of shifts in the adaptive regime of somatic growth. We also explored the evolution of the allometric relationship between body size and growth. Our results show that the evolution of fast growth trajectories in reef fishes has been considerably more common than the evolution of slow growth trajectories. Many reef fish lineages shifted towards faster growth and smaller body size evolutionary optima in the Eocene (56-33.9 million years ago), pointing to a major expansion of life history strategies in this Epoch. Of all lineages examined, the small-bodied, high-turnover cryptobenthic fishes shifted most towards extremely high growth optima, even after accounting for body size allometry. These results suggest that the high global temperatures of the Eocene5 and subsequent habitat reconfigurations6 might have been critical for the rise and retention of the highly productive, high-turnover fish faunas that characterize modern coral reef ecosystems.

Phenotypic plasticity evolves at multiple biological levels in response to environmental predictability in a long-term experiment with a halotolerant microalga.

Phenotypic plasticity, the change in the phenotype of a given genotype in response to its environment of development, is a ubiquitous feature of life, enabling organisms to cope with variation in their environment. Theoretical studies predict that, under stationary environmental variation, the level of plasticity should evolve to match the predictability of selection at the timing of development. However, the extent to which patterns of evolution of plasticity for more integrated traits are mirrored by their underlying molecular mechanisms remains unclear, especially in response to well-characterized selective pressures exerted by environmental predictability. Here, we used experimental evolution with the microalgae Dunaliella salina under controlled environmental fluctuations, to test whether the evolution of phenotypic plasticity in responses to environmental predictability (as measured by the squared autocorrelation ρ2) occurred across biological levels, going from DNA methylation to gene expression to cell morphology. Transcriptomic analysis indicates clear effects of salinity and ρ2 × salinity interaction on gene expression, thus identifying sets of genes involved in plasticity and its evolution. These transcriptomic effects were independent of DNA methylation changes in cis. However, we did find ρ2-specific responses of DNA methylation to salinity change, albeit weaker than for gene expression. Overall, we found consistent evolution of reduced plasticity in less predictable environments for DNA methylation, gene expression, and cell morphology. Our results provide the first clear empirical signature of plasticity evolution at multiple levels in response to environmental predictability, and highlight the importance of experimental evolution to address predictions from evolutionary theory, as well as investigate the molecular basis of plasticity evolution.