Evolution of Boldness and Exploratory Behavior in Giant Mice from Gough Island.
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ABSTRACT:
SUBMITTER: Stratton JA
PROVIDER: S-EPMC8716023 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Background: Island populations repeatedly evolve extreme body sizes, but the genomic basis of this morphological pattern remains largely unknown. To understand how organisms on islands evolve gigantism, we compared genome-wide patterns of gene expression in Gough Island mice, the largest wild house mice in the world, and mice from the WSB/EiJ wild-derived inbred strain. In a highly replicated experiment, we used RNASeq to quantify differences in gene expression in three key metabolic organs: gonadal adipose depot, hypothalamus, and liver. Results: We discovered pervasive evidence of transcriptional evolution, with 20% or more of differentially regulated transcripts in each organ exhibiting expression fold changes of at least 2X. By considering differential expression jointly with the genomic positions of quantitative trait loci for body size and single nucleotide differences located within established tissue-specific regulatory elements, we nominated 66 candidate genes for extreme size evolution, including Irs1 and Lrp1. Patterns of differential expression across three developmental time points in the liver revealed that Arid5b potentially regulates tens of co-regulated gene groups. Functional enrichment analyses on thousands of differentially expressed genes pointed to cell cycling, mitochondrial function, signaling pathways, immune reactivity, and nutrient metabolism as potential causes of weight accumulation in Gough Island mice. Conclusion: Collectively, our results suggest that extensive regulatory evolution in metabolic organs contributed to the rapid evolution of gigantism during the short time house mice have inhabited Gough Island.
2020-09-18 | GSE135007 | GEO
Project description:A key challenge in understanding how organisms adapt to their environments is to identify the mutations and genes that make it possible. By comparing patterns of sequence variation to neutral predictions across genomes, the targets of positive selection can be located. We applied this logic to house mice that invaded Gough Island, an unusual population that shows phenotypic and ecological hallmarks of selection. We used massively parallel short-read sequencing to survey the genomes of 14 Gough Island mice. We computed a set of summary statistics to capture diverse aspects of variation across these genome sequences, used approximate Bayesian computation to reconstruct a null demographic model, and then applied machine learning to estimate the posterior probability of positive selection in each region of the genome. Using a conservative threshold, 1,463 5kb windows show strong evidence for positive selection in Gough Island mice but not in a mainland reference population of German mice. Disproportionate shares of these selection windows contain genes that harbor derived nonsynonymous mutations with large frequency differences. Over-represented gene ontologies in selection windows emphasize neurological themes. Inspection of genomic regions harboring many selection windows with high posterior probabilities pointed to genes with known effects on exploratory behavior and body size as potential targets. Some genes in these regions contain candidate adaptive variants, including missense mutations and/or putative regulatory mutations. Our results provide a genomic portrait of adaptation to island conditions and position Gough Island mice as a powerful system for understanding the genetic component of natural selection.
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Project description:Nucleoredoxin is a thioredoxin-like redoxin that has been recognized as redox modulator of WNT signaling. Using a Yeast-2-Hybrid screen, we identified calcium calmodulin kinase 2a, Camk2a, as a prominent prey in a brain library. Camk2a is crucial for nitric oxide dependent processes of neuronal plasticity of learning and memory. Therefore, the present study assessed functions of NXN in neuronal Nestin-NXN-/- deficient mice. The NXN-Camk2a interaction was confirmed by coimmunoprecipitation, and by colocalization in neuropil and dendritic spines. Functionally, Camk2a activity was reduced in NXN deficient neurons and restored with recombinant NXN. Proteomics revealed reduced oxidation in the hippocampus of Nestin-NXN-/- deficient mice, including Camk2a, further synaptic and mitochondrial proteins, and was associated with a reduction of mitochondrial respiration. Nestin-NXN-/- mice were healthy and behaved normally in behavioral tests of anxiety, activity and sociability. They had no cognitive deficits in touchscreen based learning & memory tasks, but omitted more trials showing a lower interest in the reward. They also engaged less in rewarding voluntary wheel running, and in exploratory behavior in IntelliCages. Accuracy was enhanced owing to the loss of exploration. The data suggested that NXN maintained the oxidative state of Camk2a and thereby its activity. In addition, it supported oxidation of other synaptic and mitochondrial proteins, and mitochondrial respiration. The loss of NXN-dependent pro-oxidative functions manifested in a loss of exploratory drive and reduced interest in reward in behaving mice.
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Project description:Island populations repeatedly evolve extreme body sizes, but the genomic basis of this pattern remains largely unknown. To understand how organisms on islands evolve gigantism, we compared genome-wide patterns of gene expression in Gough Island mice, the largest wild house mice in the world, and mainland mice from the WSB/EiJ wild-derived inbred strain. We used RNA-seq to quantify differential gene expression in three key metabolic organs: gonadal adipose depot, hypothalamus, and liver. Between 4,000 and 8,800 genes were significantly differentially expressed across the evaluated organs, representing between 20% and 50% of detected transcripts, with 20% or more of differentially expressed transcripts in each organ exhibiting expression fold changes of at least 2×. A minimum of 73 candidate genes for extreme size evolution, including Irs1 and Lrp1, were identified by considering differential expression jointly with other data sets: 1) genomic positions of published quantitative trait loci for body weight and growth rate, 2) whole-genome sequencing of 16 wild-caught Gough Island mice that revealed fixed single-nucleotide differences between the strains, and 3) publicly available tissue-specific regulatory elements. Additionally, patterns of differential expression across three time points in the liver revealed that Arid5b potentially regulates hundreds of genes. Functional enrichment analyses pointed to cell cycling, mitochondrial function, signaling pathways, inflammatory response, and nutrient metabolism as potential causes of weight accumulation in Gough Island mice. Collectively, our results indicate that extensive gene regulatory evolution in metabolic organs accompanied the rapid evolution of gigantism during the short time house mice have inhabited Gough Island.
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Project description:While rat ultrasonic vocalizations (USVs) are known to vary with anticipation of an aversive vs. positive stimulus, little is known about USVs in adult mice in relation to behaviors. We recorded the calls of adult C57BL/6J male mice under different environmental conditions by exposing mice to both novel and familiar environments that varied in stress intensity through the addition of bright light or shallow water. In general, mouse USVs were significantly more frequent and of longer duration in novel environments. Particularly, mice in dimly-lit novel environments performed more USVs while exhibiting unsupported rearing and walking behavior, and these calls were mostly at high frequency. In contrast, mice exhibited more low frequency USVs when engaging in supported rearing behavior in novel environments. These findings are consistent with data from rats suggesting that low-frequency calls are made under aversive conditions and high-frequency calls occur in non-stressful conditions. Our findings increase understanding of acoustic signals associated with exploratory behaviors relevant to cognitive and motivational aspects of behavior.
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Project description:Giant island mice exhibit widespread gene regulatory evolution in key metabolic organs
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Project description:Group living has been proposed to yield benefits that enhance fitness above the level that would be achieved through living as solitary individuals. Dominance hierarchies occur commonly in these social assemblages, and result, by definition, in resources not being evenly distributed between group members. Determinants of rank within a dominance hierarchy can be associated with morphological characteristics, previous experience of the individual, or personality traits such as exploration tendencies. The purpose of this study was to investigate whether greater exploration and positive responses to novel objects in homing pigeons (Columba livia) measured under laboratory conditions were associated with (i) greater initial exploration of the local area around the home loft during spontaneous exploration flights (SEF), (ii) faster and more efficient homing flights when released from further afield, and (iii) whether the traits of greater exploration and more positive responses to novel objects were more likely to be exhibited by the more dominant individuals within the group. There was no relationship between laboratory-based novel object exploration and position within the dominance hierarchy. Pigeons that were neophobic under laboratory conditions did not explore the local area during SEF opportunities. When released from sites further from home, neophobic pigeons took longer routes to home compared to those birds that had not exhibited neophobic traits under laboratory conditions, and had spontaneously explored to a greater extent. The lack of exploration in the neophobic birds is likely to have resulted in the increased costs of homing following release: unfamiliarity with the landscape likely led to the greater distances travelled and less efficient routes taken. Birds that demonstrated a lack of neophobia were not the dominant individuals inside the loft, and thus would have less access to resources such as food and potentially mates. However, a lack of neophobia makes the subordinate position possible, because subordinate birds that incur high travel costs would become calorie restricted and lose condition. Our results address emerging questions linking individual variation in behaviour with energetics and fitness consequences.This article is part of the themed issue 'Physiological determinants of social behaviour in animals'.
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Project description:Environmental enrichment confers numerous benefits when implemented in murine models and can reduce behavioral symptomatology in models of disease, such as autism spectrum disorder (ASD). However, previous work did not examine the impact of early-life environmental enrichment on each core feature of ASD. We thus implemented a social and physical enrichment at birth, modeling a semi-natural housing, and examined its impact on communicative, social, sensory, and repetitive behaviors using BTBR (autistic-like) and C57BL/6 J (B6, wildtype) mice, comparing them to standard housing conditions. We found that environmental enrichment alleviated the social deficit of juvenile BTBR mice and reduced their repetitive exploratory behavior but did not affect their rough versus smooth texture preference nor the number of maternal isolation-induced pup calls. Environmental enrichment only affected the call characteristics of B6 mice. One interpretation of these data is that early-life environmental enrichment has significant therapeutic potential to treat selective core features of ASD. Another interpretation is that reducing environmental complexity causes selective behavioral deficits in ASD-prone mice suggesting that current standard housing may be suboptimal. Overall, our data illustrate the extent to which the environment influences behavior and highlights the importance of considering housing conditions when designing experiments and interpreting behavioral results.
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