Sex-specific developmental plasticity in response to yolk corticosterone in an oviparous lizard

Corticosterone exposure during prenatal development as a result of maternal upregulation of circulating hormone levels has been shown to have effects on offspring development in mammals. Corticosterone has also been documented in egg yolk in oviparous vertebrates, but the extent to which this influences phenotypic development is less studied. We show that maternal corticosterone is transferred to egg yolk in an oviparous lizard (the mallee dragon, Ctenophorus fordi Storr), with significant variation among clutches in hormone levels. Experimental elevation of yolk corticosterone did not affect hatching success, incubation period or offspring sex ratio. However, corticosterone did have a sex-specific effect on skeletal growth during embryonic development. Male embryos exposed to relatively high levels of corticosterone were smaller on average than control males at hatching whereas females from hormone-treated eggs were larger on average than control females. The data thus suggest that males are not just more sensitive to the detrimental effects of corticosterone but rather that the sexes may have opposite responses to corticosterone during development. Positive selection on body size at hatching for both sexes in this species further suggests that increased corticosterone in egg yolk may have sex-specific fitness consequences, with potential implications for sex allocation and the evolution of hormone-mediated maternal effects.<br /

Neutral and adaptive explanations for an association between caste-biased gene expression and rate of sequence evolution

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A field experiment reveals seasonal variation in the Daphnia gut microbiome

The gut microbiome is increasingly recognized for its impact on host fitness, but it remains poorly understood how naturally variable environments influence gut microbiome diversity and composition. We studied changes in the gut microbiome of ten genotypes of water fleas Daphnia magna in submerged mesocosm enclosures in a eutrophic lake over a period of 16 weeks, from early summer to autumn. The microbial diversity increased when Daphnia were reintroduced from the laboratory to the lake, and the composition of gut microbes drastically changed. Both gut microbiome diversity and composition continued to change over the 16-week period, with alpha diversity peaking in late summer. The gut microbiome community was clearly distinct from that of the surrounding water, and temporal changes in the two communities were independent of each other. There were no consistent differences in the gut microbiomes among Daphnia genotypes in the lake environment. The change in gut microbiome over the season was accompanied by a decline in reproductive output and survival. There were weak, but statistically supported, effects of microbiota composition on Daphnia fitness, but there was no evidence that natural variation in microbiome diversity or composition was associated with tolerance to the cyanotoxin microcystin. We conclude that the gut microbiome of Daphnia is highly dynamic in a natural lake environment, but that host genetic effects on microbiome diversity and composition between genotypes within a population can be vanishingly small. These results emphasize that establishing the ecological effects of gut microbiota will require large-scale experiments under natural conditions

Seasonal variation in the response to a toxin-producing cyanobacteria in Daphnia

Many populations of water fleas (Daphnia) are exposed to algal blooms dominated by microcystin-producing cyanobacteria. However, the severity of these effects on Daphnia fitness remain poorly understood in natural populations. We investigated seasonal changes in body size, reproduction and survival of D. longispina individuals from five eutrophic lakes in southern Sweden. We tested whether individuals collected before, during or following algal blooms differed in their reproduction and survival when experimentally exposed to microcystin-producing cyanobacteria. The concentration of microcystin in the lakes was significantly higher during summer and autumn compared to spring, but there were substantial differences between lakes. The reproductive output of individuals declined consistently over the season, and this decline was stronger for Daphnia collected during periods of, or from lakes with, high microcystin concentration. There was little evidence that individuals adapted to the toxin over the season. The strong seasonal changes in body size, reproduction and survival in these D. longispina appear to be caused partly by variation in the abundance of toxin-producing cyanobacteria. Populations were unable to adapt sufficiently quickly during summer and autumn to recover from the negative effects of microcystin. We therefore suggest that seasonal increases in tolerance to microcystin-producing cyanobacteria have limited effects on the eco-evolutionary dynamics between Daphnia and phytoplankton

Loss of genetic diversity and increased embryonic mortality in non-native lizard populations

Many populations are small and isolated with limited genetic variation and high risk of mating with close relatives. Inbreeding depression is suspected to contribute to extinction of wild populations, but the historical and demographic factors that contribute to reduced population viability are often difficult to tease apart. Replicated introduction events in non-native species can offer insights into this problem because they allow us to study how genetic variation and inbreeding depression are affected by demographic events (e.g. bottlenecks), genetic admixture and the extent and duration of isolation. Using detailed knowledge about the introduction history of 21 nonnative populations of the wall lizard Podarcis muralis in England, we show greater loss of genetic diversity (estimated from microsatellite loci) in older populations and in populations from native regions of high diversity. Loss of genetic diversity was accompanied by higher embryonic mortality in non-native populations, suggesting that introduced populations are sufficiently inbred to jeopardize long-term viability. However, there was no statistical correlation between population-level genetic diversity and average embryonic mortality. Similarly, at the individual level, there was no correlation between female heterozygosity and clutch size, infertility or hatching success, or between embryo heterozygosity and mortality. We discuss these results in the context of human-mediated introductions and how the history of introductions can play a fundamental role in influencing individual and population fitness in non-native species

Adaptive responses to cool climate promotes persistence of a non-native lizard

Successful establishment and range expansion of non-native species often require rapid accommodation of novel environments. Here, we use common-garden experiments to demonstrate parallel adaptive evolutionary response to a cool climate in populations of wall lizards (Podarcis muralis) introduced from southern Europe into England. Low soil temperatures in the introduced range delay hatching, which generates directional selection for a shorter incubation period. Non-native lizards from two separate lineages have responded to this selection by retaining their embryos for longer before oviposition-hence reducing the time needed to complete embryogenesis in the nest-and by an increased developmental rate at low temperatures. This divergence mirrors local adaptation across latitudes and altitudes within widely distributed species and suggests that evolutionary responses to climate can be very rapid. When extrapolated to soil temperatures encountered in nests within the introduced range, embryo retention and faster developmental rate result in one to several weeks earlier emergence compared with the ancestral state. We show that this difference translates into substantial survival benefits for offspring. This should promote short- and long-term persistence of non-native populations, and ultimately enable expansion into areas that would be unattainable with incubation duration representative of the native range

Progressive, Transgenerational Changes in Offspring Phenotype and Epigenotype following Nutritional Transition

Induction of altered phenotypes during development in response to environmental input involves epigenetic changes. Phenotypic traits can be passed between generations by a variety of mechanisms, including direct transmission of epigenetic states or by induction of epigenetic marks de novo in each generation. To distinguish between these possibilities we measured epigenetic marks over four generations in rats exposed to a sustained environmental challenge. Dietary energy was increased by 25% at conception in F0 female rats and maintained at this level to generation F3. F0 dams showed higher pregnancy weight gain, but lower weight gain and food intake during lactation than F1 and F2 dams. On gestational day 8, fasting plasma glucose concentration was higher and β-hydroxybutyrate lower in F0 and F1 dams than F2 dams. This was accompanied by decreased phosphoenolpyruvate carboxykinase (PEPCK) and increased PPARα and carnitine palmitoyl transferase-1 mRNA expression. PEPCK mRNA expression was inversely related to the methylation of specific CpG dinucleotides in its promoter. DNA methyltransferase (Dnmt) 3a2, but not Dnmt1 or Dnmt3b, expression increased and methylation of its promoter decreased from F1 to F3 generations. These data suggest that the regulation of energy metabolism during pregnancy and lactation within a generation is influenced by the maternal phenotype in the preceding generation and the environment during the current pregnancy. The transgenerational effects on phenotype were associated with altered DNA methylation of specific genes in a manner consistent with induction de novo of epigenetic marks in each generation

Environmentally induced DNA methylation is inherited across generations in an aquatic keystone species

Transgenerational inheritance of environmentally induced epigenetic marks can have significant impacts on eco-evolutionary dynamics, but the phenomenon remains controversial in ecological model systems. We used whole-genome bisulfite sequencing of individual water fleas (Daphnia magna) to assess whether environmentally induced DNA methylation is transgenerationally inherited. Genetically identical females were exposed to one of three natural stressors, or a de-methylating drug, and their offspring were propagated clonally for four generations under control conditions. We identified between 70 and 225 differentially methylated CpG positions (DMPs) in F1 individuals whose mothers were exposed to a natural stressor. Roughly half of these environmentally induced DMPs persisted until generation F4. In contrast, treatment with the drug demonstrated that pervasive hypomethylation upon exposure is reset almost completely after one 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 freshwater communities

Chromosome-level genome assembly of Lilford's wall lizard, Podarcis lilfordi (Günther, 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 translating into 38,615 proteins. Comparison to the genome of the related species Podarcis muralis revealed substantial similarity in genome size, annotation metrics, repeat content, and a 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.This study was supported by the Institut d’Estudis Catalans under the Catalan Initiative for the Earth Biogenome Project (PRO2020-S02 to L.B.), the Swedish Research Council (VR 2017-03846 and VR-2021-04656 to T.U. and VR-2020-03650 to N.F.) and Starting Grant from the European Research Council (no. 948126 to N.F.). We also acknowledge the support of the Spanish Ministry of Science and Innovation to the EMBL partnership, the Centro de Excelencia Severo Ochoa, the CERCA Programme/Generalitat de Catalunya, the Spanish Ministry of Science and Innovation through the Instituto de Salud Carlos III and the Generalitat de Catalunya through Departament de Salut and Departament d’Empresa i Coneixement. Co-financing funds were obtained from the European Regional Development Fund by the Spanish Ministry of Science and Innovation corresponding to the Programa Operativo FEDER Plurirregional de España (POPE) 2014-2020 and by the Secretaria d’Universitats i Recerca, Departament d’Empresa i Coneixement of the Generalitat de Catalunya corresponding to the Programa Operatiu FEDER de Catalunya 2014-2020.Peer reviewe