Biology subjects

Uller, T.

Publications and source records attributed to Uller, T..

13 recordsLinked to original sources

bioRxiv2025

Neural crest cell biology shapes lizard skull evolution across evolutionary time scales

The vertebrate skull originates from two embryonic lineages, the mesoderm and the neural crest, offering a unique framework to study how developmental mechanisms connect phenotypic variation and evolutionary diversification. Using 3D geometric morphometrics, we analysed skull shape variation in lacertid lizards. Mesoderm- and neural crest-derived bones formed distinct, conserved modules at both micro- and macroevolutionary scales. In the common wall lizard (Podarcis muralis), rapid evolution of skull shape under sexual selection was primarily driven by neural crest-derived bones. While the primary axis of shape divergence in P. muralis aligned with a major axis of variation across lacertids, neural crest-derived bones exhibited slower evolutionary rates and lower morphological disparity than mesodermal-derived bones. We propose that this discrepancy between the role of the neural crest for skull evolution on micro- and macroevolution reflects constraints imposed by neural crest cell biology: although developmental plasticity enables rapid, correlated responses under sexual selection, pleiotropy may limit long-term evolvability of neural crest-derived skull regions. Teaser textThe bones of the vertebrate skull come from two developmental sources: the mesoderm and the neural crest. This dual origin allows to study how development influences evolution. Using 3D models of lizard skulls--including a species with exaggerated male traits linked to the neural crest--we examined patterns of skull variation. We found that neural crest-derived bones contribute to rapid changes driven by sexual selection. However, across different species, these same skull regions evolve more slowly and show less variation. This suggests that while neural crest cells may constrain long-term evolution because of their wide influence, they can also enable fast adaptations. The developmental biology of a trait therefore shapes its evolution.

evolutionary biology↗

bioRxiv2024

Reproductive and ecological adaptations to climate underpin the evolution of sociality in lizards

Identifying the environmental factors associated with group living is important for understanding how social systems originate, persist and diversify. In endothermic birds and mammals, living in social groups is associated with habitat constraints and harsh climatic conditions. We use phylogenetic comparative analyses to test whether climate and habitat have played similar roles in the evolution of social grouping in a globally distributed clade of ectothermic vertebrates, lizards (Nspecies = 1696). Social grouping was strongly associated with cool, dry climates across the lizard phylogeny. However, this climatic signature arose indirectly, by association with live birth (common in cool climates) and a reliance on rock crevices (common in dry climates), traits which increase parent-offspring associations and reduce offspring dispersal. In contrast, direct effects of cool temperature on the evolution of social grouping were marginal and restricted to live bearing species. Our results demonstrate that relationships between climate and sociality may result from climatic adaptations that go on to promote the emergence of grouping behaviour.

evolutionary biology↗

bioRxiv2023

Using developmental dynamics for evolutionary prediction and control

Understanding, predicting, and controlling the phenotypic consequences of genetic and environmental change is essential to many areas of fundamental and applied biology. In evolutionary biology, the generative process of development is a major source of organismal evolvability that constrains or facilitates adaptive change by shaping the distribution of phenotypic variation that selection can act upon. While the complex interactions between genetic and environmental factors during development may appear to make it impossible to infer the consequences of perturbations, the persistent observation that many perturbations result in similar phenotypes indicates that there is a logic to what variation is generated. Here, we show that a general representation of development as a dynamical system can reveal this logic. We build a framework that allows to predict the phenotypic effects of perturbations, and conditions for when the effects of perturbations of different origin are concordant. We find that this concordance is explained by two generic features of development, namely the dynamical dependence of the phenotype on itself and the fact that all perturbations must be funneled by the same developmental process. We apply our theoretical results to classical models of development and show that it can be used to predict the evolutionary response to selection using information of plasticity, and to accelerate evolution in a desired direction. The framework we introduce provides a way to quantitatively interchange perturbations, opening a new avenue of perturbation design to control the generation of variation, and thus evolution.

evolutionary biology↗

bioRxiv2023

How do fluctuating temperatures alter the cost of development?

O_LIQuantifying how variable temperature regimes affect energy expenditure during development is crucial for understanding how future thermal regimes may impact early life survival and population persistence. C_LIO_LIDevelopmental Cost Theory (DCT) suggests that there is an optimal temperature (Topt) that minimises energy expenditure during development (the "cost of development"). Exposure to fluctuating temperatures around an average of Topt are anticipated to increase either development time or metabolic rate. As a result, embryos will rapidly deplete yolk reserves, and consequently hatch at a smaller size or with less residual yolk to support postnatal survival and growth. C_LIO_LIHere, we studied total embryonic energy expenditure (development time and rate of CO2 production) and conversion of yolk into tissue in common wall lizards (Podarcis muralis) under three incubation treatments anticipated, based on DCT, to increase the cost of development: no variance (Topt constant, 24 {degrees}C), low variance (22 - 26 {degrees}C), and high variance (18 - 30 {degrees}C). C_LIO_LIAs predicted, we found that increasing variance around Topt increased the cost of development, despite reducing time to hatching. As a consequence, embryos on average hatched with 59% lower residual yolk reserves under high variance versus constant incubation temperatures. C_LIO_LIOur results highlight how the relative temperature sensitivities of development time and metabolic rate determine the cost of development, which in turn may predict the ability of egg-laying ectotherms to persist in variable environments. We show that DCT can provide a mechanistic framework for understanding the widespread, but often seemingly idiosyncratic, effects of fluctuating incubation temperatures on hatchling tissue and residual yolk mass. C_LI

physiology↗

bioRxiv2023

Chromosome-level genome assembly of Lilford's wall lizard, Podarcis lilfordi (Gunther, 1874) from the Balearic Islands (Spain)

The Mediterranean lizard Podarcis lilfordi is an emblematic species of the Balearic Islands. The extensive phenotypic diversity among extant isolated populations makes the species a great insular model system for eco-evolutionary studies, as well as a challenging target for conservation management plans. Here we report the first high quality chromosome-level assembly and annotation of the P. lilfordi genome, along with its mitogenome, based on a mixed sequencing strategy (10X Genomics linked reads, Oxford Nanopore Technologies long reads and Hi-C scaffolding) coupled with extensive transcriptomic data (Illumina and PacBio). The genome assembly (1.5 Gb) is highly contiguous (N50 = 90 Mb) and complete, with 99% of the sequence assigned to candidate chromosomal sequences and >97% gene completeness. We annotated a total of 25,663 protein-coding genes, assigning 72% to known functions. Comparison to the genome of the related species Podarcis muralis revealed substantial similarity in genome size, annotation metrics, repeat content, and strong collinearity, despite their evolutionary distance (~18-20 MYA). This genome expands the repertoire of available reptilian genomes and will facilitate the exploration of the molecular and evolutionary processes underlying the extraordinary phenotypic diversity of this insular species, while providing a critical resource for conservation genomics.

genomics↗

bioRxiv2022

Population divergence in maternal investment and embryo energy use and allocation reveals adaptive responses to cool climates

The thermal sensitivity of early life stages can play a fundamental role in constraining species distribution. For egg-laying ectotherms, cool temperatures often extend development time and exacerbate developmental energy cost. Despite these costs, egg laying is still observed at high latitudes and altitudes. How embryos overcome the developmental constraints posed by cool climates is crucial knowledge for explaining the persistence of oviparous species in such environments and for understanding thermal adaptation more broadly. Here, we studied maternal investment, and embryo energy use and allocation in wall lizards spanning altitudinal regions, as potential mechanisms of local adaptation to development in cool climates. Specifically, we compared population-level differences in (1) investment from mothers (egg mass, embryo retention and thyroid yolk hormone concentration), (2) embryo energy expenditure during development, and (3) embryo energy allocation from yolk towards tissue. We found evidence that energy expenditure was greater under cool compared with warm incubation temperatures. Females from relatively cool regions did not compensate for this energetic cost of development by producing larger eggs or increasing thyroid hormone concentration in yolk. Instead, embryos from the high-altitude region used less energy to complete development, i.e., they developed faster without a concomitant increase in metabolic rate, compared with those from the low-altitude region. Embryos from high altitudes also allocated relatively more energy towards tissue production, hatching with lower residual yolk:tissue ratios than low-altitude region embryos. These results suggest that local adaptation to cool climate in wall lizards involves mechanisms that regulate embryonic utilisation of yolk reserves and its allocation towards tissue, rather than shifts in maternal investment of yolk content or composition.

evolutionary biology↗

bioRxiv2021

Environmentally-induced DNA methylation is inherited across generations in an aquatic keystone species (Daphnia magna)

Environmental stress can result in epigenetic modifications that are passed down several generations. Such epigenetic inheritance can have significant impact on eco-evolutionary dynamics, but the phenomenon remains controversial in ecological model systems. Here, we used whole-genome bisulfite sequencing on individual water fleas (Daphnia magna) to assess whether environmentally-induced DNA methylation can persist for up to four generations. Genetically identical females were exposed to a control treatment, one of three natural stressors (high temperature, zinc, microcystin), or the methylation-inhibitor 5-azacytidine. After exposure, lines were propagated clonally for four generations under control conditions. We identified between 70 and 225 differentially methylated CpG positions (DMPs) between controls and F1 individuals whose mothers (and therefore they themselves as germ cells) were exposed to one of the three natural stressors. Between 46% and 58% of these environmentally-induced DMPs persisted until generation F4 without attenuation in their magnitude of differential methylation. DMPs were enriched in exons and largely stressor-specific, suggesting a possible role in environment-dependent gene regulation. In contrast, treatment with the compound 5-azacytidine demonstrated that pervasive hypo-methylation upon exposure is reset almost completely after a single generation. These results suggest that environmentally-induced DNA methylation is non-random and stably inherited across generations in Daphnia, making epigenetic inheritance a putative factor in the eco-evolutionary dynamics of fresh-water communities. Author summaryWater fleas are important keystone species mediating eco-evolutionary dynamics in lakes and ponds. It is currently an open question in how far epigenetic inheritance contributes to the ability of Daphnia populations to adapt to environmental stress. Using a range of naturally occurring stressors and a multi-generational design, we show that environmentally-induced DNA methylation variants are stably inherited for at least four generations in Daphnia magna. The induced variation in DNA methylation are stressor-specific and almost exclusively found in exons, bearing the signatures of functional adaptations. Our findings imply that ecological adaptations of Daphnia to seasonal fluctuations can be underpinned by epigenetic inheritance of DNA methylation without changes in gene frequencies.

evolutionary biology↗

bioRxiv2021

Population genomics of wall lizards reflects the dynamic history of the Mediterranean Basin

The Mediterranean Basin has experienced extensive change in geology and climate over the past six million years. Yet, the relative importance of key geological events for the distribution and genetic structure of the Mediterranean fauna remains poorly understood. Here, we use population genomic and phylogenomic analyses to establish the evolutionary history and genetic structure of common wall lizards (Podarcis muralis). This species is particularly informative because, in contrast to other Mediterranean lizards, it is widespread across the Iberian, Italian, and Balkan peninsulas, and in extra-Mediterranean regions. We found strong support for six major lineages within P. muralis, which were largely discordant with the phylogenetic relationship of mitochondrial DNA. The most recent common ancestor of extant P. muralis was likely distributed in the Italian Peninsula, and experienced an "Out-of-Italy" expansion following the Messinian salinity crisis (~5 Mya), resulting in the differentiation into the extant lineages on the Iberian, Italian and Balkan peninsulas. Introgression analysis revealed that both inter- and intraspecific gene flow have been pervasive throughout the evolutionary history of P. muralis. For example, the Southern Italy lineage has a hybrid origin, formed through admixture between the Central Italy lineage and an ancient lineage that was the sister to all other P. muralis. More recent genetic differentiation is associated with the onset of the Quaternary glaciations, which influenced population dynamics and genetic diversity of contemporary lineages. These results demonstrate the pervasive role of Mediterranean geology and climate for the evolutionary history and population genetic structure of extant species.

evolutionary biology↗

bioRxiv2021

Behavioural adaptations in egg laying ancestors facilitate evolutionary transitions to live birth

Live birth is a key innovation that has evolved from egg laying ancestors over 100 times in reptiles. However, egg-laying lizards and snakes often possess preferred body temperatures that are lethal to developing embryos, which should select against egg retention. Here, we demonstrate that thermal mismatches between mothers and offspring are widespread across the squamate phylogeny. This mismatch is resolved by gravid females adjusting their body temperature towards the thermal optimum of embryos. Importantly, phylogenetic reconstructions suggest this thermoregulatory behaviour evolved in egg-laying species prior to the evolution of live birth. Maternal thermoregulatory behaviour therefore bypasses the constraints imposed by a slowly evolving thermal physiology and has likely been a key facilitator in the repeated transitions to live birth.

evolutionary biology↗

bioRxiv2020

Developmental models reveal the role of phenotypic plasticity in explaining genetic evolvability

Biological evolution exhibits an extraordinary capability to adapt organisms to their environments. The explanation for this often takes for granted that random genetic variation produces at least some beneficial phenotypic variation for natural selection to act on. Such genetic evolvability could itself be a product of evolution, but it is widely acknowledged that the immediate selective gains of evolvability are small on short timescales. So how do biological systems come to exhibit such extraordinary capacity to evolve? One suggestion is that adaptive phenotypic plasticity makes genetic evolution find adaptations faster. However, the need to explain the origin of adaptive plasticity puts genetic evolution back in the driving seat, and genetic evolvability remains unexplained. To better understand the interaction between plasticity and genetic evolvability, we simulate the evolution of phenotypes produced by gene-regulation network-based models of development. First, we show that the phenotypic variation resulting from genetic and environmental change are highly concordant. This is because phenotypic variation, regardless of its cause, occurs within the relatively specific space of possibilities allowed by development. Second, we show that selection for genetic evolvability results in the evolution of adaptive plasticity and vice versa. This linkage is essentially symmetric but, unlike genetic evolvability, the selective gains of plasticity are often substantial on short, including within-lifetime, timescales. Accordingly, we show that selection for phenotypic plasticity is, in general, the most efficient and results in the rapid evolution of high genetic evolvability. Thus, without overlooking the fact that adaptive plasticity is itself a product of genetic evolution, this shows how plasticity can influence adaptive evolution and helps explain the genetic evolvability observed in biological systems.

evolutionary biology↗

bioRxiv2018

Regulatory changes in pterin and carotenoid genes underlie balanced color polymorphisms in the wall lizard

Reptiles use pterin and carotenoid pigments to produce yellow, orange, and red colors. These conspicuous colors serve a diversity of signaling functions, but their molecular basis remains unresolved. Here, we show that the genomes of sympatric color morphs of the European common wall lizard, which differ in orange and yellow pigmentation and in their ecology and behavior, are virtually undifferentiated. Genetic differences are restricted to two small regulatory regions, near genes associated with pterin (SPR) and carotenoid metabolism (BCO2), demonstrating that a core gene in the housekeeping pathway of pterin biosynthesis has been co-opted for bright coloration in reptiles and indicating that these loci exert pleiotropic effects on other aspects of physiology. Pigmentation differences are explained by extremely divergent alleles and haplotype analysis revealed abundant trans-specific allele sharing with other lacertids exhibiting color polymorphisms. The evolution of these conspicuous color ornaments is the result of ancient genetic variation and cross-species hybridization.

evolutionary biology↗

bioRxiv2018

How adaptive plasticity evolves when selected against

Adaptive plasticity allows organisms to cope with environmental change, thereby increasing the populations long-term fitness. However, individual selection can only compare the fitness of individuals within each generation: if the environment changes more slowly than the generation time (i.e., a coarse-grained environment) a population will not experience selection for plasticity even if it is adaptive in the long-term. How does adaptive plasticity then evolve? One explanation is that, if competing alleles conferring different degrees of plasticity persist across multiple environments, natural selection between lineages carrying those alleles could select for adaptive plasticity (lineage selection).\n\nWe show that adaptive plasticity can evolve even in the absence of such lineage selection. Instead, we propose that adaptive plasticity in coarse-grained environments evolves as a by-product of inefficient short-term natural selection. In our simulations, populations that can efficiently respond to selective pressures follow short-term, local, optima and have lower long-term fitness. Conversely, populations that accumulate limited genetic change within each environment evolve long-term adaptive plasticity even when plasticity incurs short-term costs. These results remain qualitatively similar regardless of whether we decrease the efficiency of natural selection by increasing the rate of environmental change or decreasing mutation rate, demonstrating that both factors act via the same mechanism. We demonstrate how this mechanism can be understood through the concept of learning rate.\n\nOur work shows how plastic responses that are costly in the short term, yet adaptive in the long term, can evolve as a by-product of inefficient short-term selection, without selection for plasticity at either the individual or lineage level.

evolutionary biology↗

bioRxiv2018

Epigenetic selection and the DNA methylation signatures of adverse prenatal environments

Maternal adversity is associated with long-term physiological changes in offspring. These are believed to be mediated through epigenetic mechanisms, including DNA methylation (DNAm). Changes in DNAm are often interpreted as damage or as part of plastic responses of the embryo. We propose that selection on stochastic DNAm differences generated during epigenetic reprogramming after fertilization contributes to the effects of maternal adversity on DNAm. Using a mathematical model of epigenetic reprogramming in the early embryo we predict that this \"epigenetic selection\" will generate a characteristic reduction in variance of DNAm at selected loci in populations exposed to maternal adversity. We tested this prediction using DNAm data from a human cohort prenatally exposed to the Dutch Famine and confirmed the reduction in DNAm variance, suggesting that epigenetic selection may have occurred. Epigenetic selection should be considered as a possible mechanism linking adversity in pregnancy to offspring health and may have implications for the likely effectiveness of intervention strategies.

epidemiology↗