Metamorphosis imposes variable constraints on genome expansion through effects on development

Rl, Mueller; Cressler, Clayton E.; Rs, Schwarz; Ra, Chong; Butler, Marguerite A.

doi:10.1101/2021.05.05.442795

Cited by 6 publications

(4 citation statements)

References 142 publications

(250 reference statements)

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“…Our results suggest that these transitions may be critical periods of viability selection, whether genetic effects on survival are mediated by genome-wide heterozygosity or by specific loci. Likewise, this finding leads to the novel hypothesis that viability selection may be more common and stronger among species and lineages that undergo metamorphosis or other discrete life stage transitions than among species and lineages that do not undergo these transitions (Mueller et al, 2023;ten Brink et al, 2019;Truman, 2019).…”

Section: Discussionmentioning

confidence: 96%

Outbreeding reduces survival during metamorphosis in a headwater stream salamander

Lowe,

Addis,

Cochrane

2024

Molecular Ecology

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Assessing direct fitness effects of individual genetic diversity is challenging due to the intensive and long‐term data needed to quantify survival and reproduction in the wild. But resolving these effects is necessary to determine how inbreeding and outbreeding influence eco‐evolutionary processes. We used 8 years of capture–recapture data and single nucleotide polymorphism genotypes for 1906 individuals to test for effects of individual heterozygosity on stage‐specific survival probabilities in the salamander Gyrinophilus porphyriticus. The life cycle of G. porphyriticus includes an aquatic larval stage followed by metamorphosis into a semi‐aquatic adult stage. In our study populations, the larval stage lasts 6–10 years, metamorphosis takes several months, and lifespan can reach 20 years. Previous studies showed that metamorphosis is a sensitive life stage, leading us to predict that fitness effects of individual heterozygosity would occur during metamorphosis. Consistent with this prediction, monthly probability of survival during metamorphosis declined with multi‐locus heterozygosity (MLH), from 0.38 at the lowest MLH (0.10) to 0.06 at the highest MLH (0.38), a reduction of 84%. Body condition of larvae also declined significantly with increasing MLH. These relationships were consistent in the three study streams. With evidence of localised inbreeding within streams, these results suggest that outbreeding disrupts adaptations in pre‐metamorphic and metamorphic individuals to environmental gradients along streams, adding to evidence that headwater streams are hotspots of microgeographic adaptation. Our results also underscore the importance of incorporating life history in analyses of the fitness effects of individual genetic diversity and suggest that metamorphosis and similar discrete life stage transitions may be critical periods of viability selection.

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Section: Discussionmentioning

confidence: 96%

Outbreeding reduces survival during metamorphosis in a headwater stream salamander

Lowe,

Addis,

Cochrane

2024

Molecular Ecology

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“…This might suggest that the limb regeneration and slow aging phenotypes in salamanders are associated with the substantially larger amounts of heterochromatin in their genomes compared to other species with smaller genomes. Obligate neotenes consistently have genomes much larger than metamorphic or direct developing salamanders [97,98]. Larger amounts of heterochromatin might therefore facilitate DNA repair, slow the rate of aging, enhance MLS and retard developmental rate.…”

Section: Limb Regeneration Cell Differentiation Development and Agingmentioning

confidence: 99%

DNA Damage, Genome Stability and Adaptation: a Question of Chance or Necessity?

Herrick

2024

Preprint

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DNA damage causes the mutations that are the principal source of genetic variation. DNA damage detection and repair mechanisms therefore play a determining role in generating the genetic diversity on which natural selection acts. Speciation, it is commonly assumed, occurs at a rate set by the level of standing allelic diversity in a population. The process of speciation is driven by a combination of two evolutionary forces: genetic drift and ecological selection. Genetic drift takes place under conditions of relaxed selection, and results in a balance between rates of mutation and rates of genetic substitution. These two processes, drift and selection, are necessarily mediated by a variety of mechanisms guaranteeing genome stability in any given species. One of the outstanding questions in evolutionary biology concerns the origin of the widely varying phylogenetic distribution of biodiversity across the tree of life, and how the forces of drift and selection contribute to shaping that distribution. The following examines some of the molecular mechanisms underlying genome stability and the adaptive radiations that are associated with biodiversity and the widely varying species richness and evenness in the different eukaryotic lineages.

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“…Consequently, salamander genomes are of extensive interest for numerous topics including the genetic basis of evolutionary differences in life history and genome size (Lertzman-Lepofsky et al . 2019; Mueller et al . 2023), as well as regeneration, vision, and immunity (Roth et al .…”

Section: Introductionmentioning

confidence: 99%

The first complete assembly for a lungless urodelan with a "miniaturized" genome, the Northern Dusky Salamander (Plethodontidae: Desmognathus fuscus)

Myers,

Pyron

2024

Preprint

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Salamanders have some of the largest genomes among animals. However, there is a great disparity in total size, ranging from ~8-120GB depending on the lineage. Species in the lungless genus Desmognathus (Plethodontidae) are among the smallest, with estimated genome sizes of 13-15GB. Salamander genomes have exceptional interest in numerous topics ranging from genome-size evolution, the genetic basis of evolutionary differences in life history, and the physiological basis of regeneration, vision, and immunity. However, their large genomes have limited previous attempts at sequencing and assembly, particularly given the difficulties of mapping extensive repeat regions with short-read data. Here we assemble a draft genome of Desmognathus fuscus using PacBio HiFi reads and generate transcriptomic data from two specimens. The combined assembly resulted in a 16.1GB genome in 19,640 contigs and an N/L50 of 2,455/1.75MB, with the longest contig at 27.9MB. The assembly and transcriptome are nearly complete with 93% of the 5,310 BUSCO tetrapod orthologs identified. Attempts to scaffold these data to the existing Ambystoma genome resulted in only 5.8GB of the D. fuscus genome mapping to this reference. This low success suggests substantial syntenic and sequence divergence across salamanders, which may be the result of significant miniaturization in the Desmognathus genome. Identification and annotation of transposable elements reveals that only 26% of the genome is single copy with 74% corresponding to TEs. The most common class of TE in the genome are LTRs (35% of the total genome) and LINEs (~15% of the genome). The relative divergence landscape of these TEs shows an early expansion and slow contraction of LINEs, followed by a quick recent expansion of both LTRs and DNA transposons. This assembly will serve as an important reference for amphibian genomics.

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Metamorphosis imposes variable constraints on genome expansion through effects on development

Cited by 6 publications

References 142 publications

Outbreeding reduces survival during metamorphosis in a headwater stream salamander

Outbreeding reduces survival during metamorphosis in a headwater stream salamander

DNA Damage, Genome Stability and Adaptation: a Question of Chance or Necessity?

The first complete assembly for a lungless urodelan with a "miniaturized" genome, the Northern Dusky Salamander (Plethodontidae: Desmognathus fuscus)

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