Extracellular matrix materials known as perineuronal nets (PNNs) have been shown to have remarkable consequences for the maturation of neural circuits and stabilization of behavior. It has been proposed that, due to the possibly long‐lived biochemical nature of their components, PNNs may be an important substrate by which long‐term memories are stored in the central nervous system. However, little empirical evidence exists that shows that PNNs are themselves stable once established. Thus, the question of their temporal dynamics remains unresolved. We leverage the dramatic morphological and behavioral transformations that occur during amphibian metamorphosis to show that PNNs can be highly dynamic in nature. We used established lectin histochemistry to show that PNNs undergo drastic reconstruction during the metamorphic transition. Pre‐metamorphic tadpoles have abundant lectin‐labeled pericellular material, which we interpret to be PNNs, surrounding neurons throughout the central nervous system. During the metamorphic transition, these structures degrade, and begin to reform in the months following metamorphosis. We show that PNN sizes and staining intensity further change over metamorphosis, suggesting compositional rearrangement. We found PNNs in brain regions with putative homology to regions in mammals with known PNN function, and in other shared regions where PNN function is unknown. Our results suggest that PNNs are susceptible to remodeling by endogenous mechanisms during development. Interpreting the roles of PNNs in circuit maturation and stability requires understanding their temporal relationship with the neurons and synapses they surround. Our work provides further impetus to investigate this relationship in tandem with developmental and behavioral studies.
Genome size varies ∼100,000-fold across eukaryotes and has long been hypothesized to be influenced by metamorphosis in animals. Transposable element accumulation has been identified as a major driver of increase, but the nature of constraints limiting the size of genomes has remained unclear, even as traits such as cell size and rate of development co-vary strongly with genome size. Salamanders, which possess diverse metamorphic and non-metamorphic life histories, join the lungfish in having the largest vertebrate genomes—3 to 40 times that of humans—as well as the largest range of variation in genome size. We tested 13 biologically-inspired hypotheses exploring how the form of metamorphosis imposes varying constraints on genome expansion in a broadly representative phylogeny containing 118 species of salamanders. We show that metamorphosis during which animals undergo the most extensive and synchronous remodeling imposes the most severe constraint against genome expansion, with the severity of constraint decreasing with reduced extent and synchronicity of remodeling. More generally, our work demonstrates the potential for broader interpretation of phylogenetic comparative analysis in exploring the balance of multiple evolutionary pressures shaping phenotypic evolution.
more » « less- Award ID(s):
- 1911585
- NSF-PAR ID:
- 10410777
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Integrative Organismal Biology
- Volume:
- 5
- Issue:
- 1
- ISSN:
- 2517-4843
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract -
Transposable elements (TEs) are sequences that replicate and move throughout genomes, and they can be silenced through methylation of cytosines at CpG dinucleotides. TE abundance contributes to genome size, but TE silencing variation across genomes of different sizes remains underexplored. Salamanders include most of the largest C-values – 9 to 120 Gb. We measured CpG methylation levels in salamanders with genomes ranging from 2N = ∼58 Gb to 4N = ∼116 Gb. We compared these levels to results from endo- and ectothermic vertebrates with more typical genomes. Salamander methylation levels are approximately 90%, higher than all endotherms. However, salamander methylation does not differ from other ectotherms, despite an approximately 100-fold difference in nuclear DNA content. Because methylation affects the nucleotide compositional landscape through 5-methylcytosine deamination to thymine, we quantified salamander CpG dinucleotide levels and compared them to other vertebrates. Salamanders and other ectotherms have comparable CpG levels, and ectotherm levels are higher than endotherms. These data show no shift in global methylation at the base of salamanders, despite a dramatic increase in TE load and genome size. This result is reconcilable with previous studies that considered endothermy and ectothermy, which may be more important drivers of methylation in vertebrates than genome size.more » « less
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Summary Plastid evolution has been attributed to a single primary endosymbiotic event that occurred about 1.6 billion years ago (BYA) in which a cyanobacterium was engulfed and retained by a eukaryotic cell, although early steps in plastid integration are poorly understood. The photosynthetic amoeba
Paulinella chromatophora represents a unique model for the study of plastid evolution because it contains cyanobacterium‐derived photosynthetic organelles termed ‘chromatophores’ that originated relatively recently (0.09–0.14 BYA). The chromatophore genome is about a third the size of the genome of closely related cyanobacteria, but 10‐fold larger than most plastid genomes. Several genes have been transferred from the chromatophore genome to the host nuclear genome through endosymbiotic gene transfer (EGT). Some EGT‐derived proteins could be imported into chromatophores for function. Two photosynthesis‐related genes (psaI and csos4A ) are encoded by both the nuclear and chromatophore genomes, suggesting that EGT inPaulinella chromatophora is ongoing. Many EGT‐derived genes encode proteins that function in photosynthesis and photoprotection, including an expanded family of high‐light‐inducible (ncHLI) proteins. Cyanobacterialhli genes are high‐light induced and required for cell viability under excess light. We examined the impact of light onPaulinella chromatophora and found that this organism is light sensitive and lacks light‐induced transcriptional regulation of chromatophore genes and most EGT‐derived nuclear genes. However, several ncHLI genes have reestablished light‐dependent regulation, which appears analogous to what is observed in cyanobacteria. We postulate that expansion of the ncHLI gene family and its regulation may reflect the light/oxidative stress experienced byPaulinella chromatophora as a consequence of the as yet incomplete integration of host and chromatophore metabolisms. -
null (Ed.)Abstract The spatial distribution of population affects disease transmission, especially when shelter in place orders restrict mobility for a large fraction of the population. The spatial network structure of settlements therefore imposes a fundamental constraint on the spatial distribution of the population through which a communicable disease can spread. In this analysis we use the spatial network structure of lighted development as a proxy for the distribution of ambient population to compare the spatiotemporal evolution of COVID-19 confirmed cases in the USA and China. The Visible Infrared Imaging Radiometer Suite (VIIRS) Day/Night Band sensor on the NASA/NOAA Suomi satellite has been imaging night light at ~ 700 m resolution globally since 2012. Comparisons with sub-kilometer resolution census observations in different countries across different levels of development indicate that night light luminance scales with population density over ~ 3 orders of magnitude. However, VIIRS’ constant ~ 700 m resolution can provide a more detailed representation of population distribution in peri-urban and rural areas where aggregated census blocks lack comparable spatial detail. By varying the low luminance threshold of VIIRS-derived night light, we depict spatial networks of lighted development of varying degrees of connectivity within which populations are distributed. The resulting size distributions of spatial network components (connected clusters of nodes) vary with degree of connectivity, but maintain consistent scaling over a wide range (5 × to 10 × in area & number) of network sizes. At continental scales, spatial network rank-size distributions obtained from VIIRS night light brightness are well-described by power laws with exponents near −2 (slopes near −1) for a wide range of low luminance thresholds. The largest components (10 4 to 10 5 km 2 ) represent spatially contiguous agglomerations of urban, suburban and periurban development, while the smallest components represent isolated rural settlements. Projecting county and city-level numbers of confirmed cases of COVID-19 for the USA and China (respectively) onto the corresponding spatial networks of lighted development allows the spatiotemporal evolution of the epidemic (infection and detection) to be quantified as propagation within networks of varying connectivity. Results for China show rapid nucleation and diffusion in January 2020 followed by rapid decreases in new cases in February. While most of the largest cities in China showed new confirmed cases approaching zero before the end of February, most of these cities also showed distinct second waves of cases in March or April. Whereas new cases in Wuhan did not approach zero until mid-March, as of December 2020 it has not yet experienced a second wave of cases. In contrast, the results for the USA show a wide range of trajectories, with an abrupt transition from slow increases in confirmed cases in a small number of network components in January and February, to rapid geographic dispersion to a larger number of components shortly before mobility reductions occurred in March. Results indicate that while most of the upper tail of the network had been exposed by the end of March, the lower tail of the component size distribution has only shown steep increases since mid-June.more » « less
