Biology subjects

Zakas, C.

Publications and source records attributed to Zakas, C..

9 recordsLinked to original sources

bioRxiv2026

Evolutionary landscapes of zygotic genome activation across animals

During early animal embryogenesis, gene expression control shifts from maternally deposited products to newly transcribed RNA through zygotic genome activation (ZGA). Although essential and universal, ZGA remains poorly understood outside a few model species. Here, we generated a transcriptomic atlas of early embryogenesis across 61 animal species from 13 phyla and used a unified computational framework to infer ZGA timing systematically. We find extensive variation in ZGA onset across animals, but show that the ratio between genome size and egg cytoplasmic volume, a proxy for the nuclear-to-cytoplasmic ratio, robustly predicts when genome activation begins. We also reveal that zygotic genes also differ from maternal transcripts in genomic architecture, function and evolutionary conservation, suggesting that ZGA follows a conserved molecular logic despite flexible transcriptomic outputs.

evolutionary biology↗

bioRxiv2025

RNAi Gene knockdown of R-opsin and F-actin in the marineannelid Streblospio benedicti by delivering dsRNA

BackgroundRNA interference (RNAi) is a genetic tool to disrupt the expression of selected genes by delivering dsRNA into a specific tissue of an organism, resulting in a gene knockdown. We apply RNAi methods to the marine polychaete Streblospio benedicti, which is a model system for studying evolutionary and developmental biology, which currently has no established methods for gene expression manipulation. ResultsHere we describe a RNAi gene knockdown methodology using two different approaches depending on developmental stage. We feed bacteria expressing dsRNA to early swimming larvae and microinject in vitro transcribed dsRNA in juveniles. We used two genes for testing: R-opsin and F-actin. For both developmental stages, gene knockdown was validated using qPCR (quantitative Real-Time PCR). For larvae, we also visualized reduction in RNA expression using Hybridization Chain Reaction (HCR) in situ hybridization. ConclusionsWe show that both larval feeding and juvenile microinjections are sufficient delivery mechanisms for dsRNA to result in a RNAi gene knockdown. The efficiency can vary depending on the gene and timing, but this is typical for RNAi based approaches.

developmental biology↗

bioRxiv2023

Comparative Hox genes expression within the dimorphic annelidStreblospio benedicti reveals patterning variation during development

Hox genes are transcriptional regulators that elicit cell positional identity along the anterior-posterior region of the body plan across different lineages of Metazoan. Comparison of Hox gene expression across distinct species reveals their evolutionary conservation, however their gains and losses in different lineages can correlate with body plan modifications and morphological novelty. We compare the expression of eleven Hox genes found within Streblospio benedicti, a marine annelid that produces two types of offspring with distinct developmental and morphological features. For these two distinct larval types, we compare Hox gene expression through ontogeny using HCR (hybridization chain reaction) probes for in-situ hybridization and RNA-seq data. We find that Hox gene expression patterning for both types is typically similar at equivalent developmental stages. However, some Hox genes have spatial or temporal differences between the larval types that are associated with morphological and life-history differences. This is the first comparison of developmental divergence in Hox genes expression within a single species and these changes reveal how body plan differences may arise in larval evolution.

developmental biology↗

bioRxiv2023

The role of heterochronic gene expression and regulatory architecture in early developmental divergence

New developmental programs can evolve through adaptive changes to gene expression. The annelid Streblospio benedicti has a developmental dimorphism, which provides a unique intraspecific framework for understanding the earliest genetic changes that take place during developmental divergence. Using comparative RNAseq through ontogeny, we find that only a small proportion of genes are differentially expressed at any time, despite major differences in larval development and life-history. These genes shift expression profiles across morphs by either turning off any expression in one morph or changing the timing or amount of gene expression. We directly connect the contributions of these mechanisms to differences in developmental processes. We examine F1 offspring-- using reciprocal crosses-- to determine maternal mRNA inheritance and the regulatory architecture of gene expression. These results highlight the importance of both novel gene expression and heterochronic shifts in developmental evolution, as well as the trans-acting regulatory factors in initiating divergence.

genetics↗

bioRxiv2022

Assortative mating and mate-choice contributes to a developmental dimorphism in Streblospio benedicti

Assortative mating, where individuals non-randomly mate with respect to phenotype or genotype, can occur when preferences between potential mates have evolved. When such mate preferences occur in a population it can drive evolutionary and phenotypic divergence. But the extent to which assortative mating, mate preference, and development are evolutionarily linked remains unclear. Here we use Streblospio benedicti, a marine annelid with a rare developmental dimorphism, to investigate if mate-choice could contribute to developmental evolution. For S. benedicti two types of ecologically and phenotypically similar adults persist in natural populations, but they give rise to distinctly different offspring with alternative lifehistories. This dimorphism persists despite the absence of post-zygotic reproductive barriers, where crosses between the developmental types can produce phenotypically intermediate offspring. How this life-history strategy evolved remains unknown, but assortative mating is a typical first step in evolutionary divergence. Here we investigate if female mate-choice is occurring in this species. We find that mate preferences could be contributing to the maintenance of alternative developmental and life-history strategies.

evolutionary biology↗

bioRxiv2022

Maternal patterns of inheritance alter transcript expression in eggs

Modifications to early development can lead to evolutionary diversification. The early stages of development are under maternal control, as mothers produce eggs loaded with nutrients, proteins and mRNAs that direct early embryogenesis. Maternally provided mRNAs are the only expressed genes in initial stages of development and are known to be tightly regulated. Differences in maternal mRNA provisioning could lead to phenotypic changes in embryogenesis and ultimately evolutionary changes in development. However, the extent to which variation in maternal mRNA provisioning impacts ontogeny or life-history is unknown. Here, we use a species with dimorphic development-- where females make eggs and larvae of different sizes and life-history modes--to investigate the extent of variation in maternal mRNA provisioning to the egg. We examine the effect of gene expression differences on subsequent generations of egg provisioning and determine the regulatory architecture underlying mRNA provisioning differences. We find that there is significant variation in gene expression across eggs of different development modes, and that both parent-of-origin and allele-specific effects contribute to mRNA expression differences. We also find that offspring of intraspecific crosses differentially provision their eggs based on their parents cross direction. This effect of allelic expression based on parent-of-origin has not been previously demonstrated in reproductive traits like oogenesis. AUTHOR SUMMARYVariation in early developmental programs can provide the basis for evolutionary diversification. In the early embryo, cellular functions are carried out by proteins and transcripts contributed by the mother to the egg until the embryos own genome can take over. Since these maternal factors are responsible for setting up all of the subsequent development of the offspring, they tend to be tightly regulated. However, variation exists in the amount and types of transcripts mothers provide. Here we examine how the variation in maternal transcripts that occurs in eggs of the species Streblospio benedicti, leads to developmental differences. S. benedicti offspring follow one of two distinct developmental programs that originate with egg size differences. We find significant variation in maternally provided transcripts correlated with the two life-histories, and that some of this variation in egg transcripts is directly related to the developmental type of the mothers own parents. This parental effect on how mothers provide transcripts to their eggs has not previously been described and indicates the possibility for an offsprings grandparents to affect their early developmental program by modulating the transcripts their mother provides.

genetics↗

bioRxiv2021

The genome of the poecilogonous annelid Streblospio benedicti

Streblospio benedicti is a common marine annelid that has become an important model for developmental evolution. It is the only known example of poecilogony, where two distinct developmental modes occur within a single species, that is due to a heritable difference in egg size. The dimorphic developmental programs and life-histories exhibited in this species depend on differences within the genome, making it an optimal model for understanding the genomic basis of developmental divergence. Studies using S. benedicti have begun to uncover the genetic and genomic principles that underlie developmental uncoupling, but until now they have been limited by the lack of availability of genomic tools. Here we present an annotated chromosomal-level genome assembly of S. benedicti generated from a combination of Illumina reads, Nanopore long reads, Chicago and Hi-C chromatin interaction sequencing, and a genetic map from experimental crosses. At 701.4 Mb, the S. benedicti genome is the largest annelid genome to date that has been assembled to chromosomal scaffolds, yet it does not show evidence of extensive gene family expansion, but rather longer intergenic regions. The complete genome of S. benedicti is valuable for functional genomic analyses of development and evolution, as well as phylogenetic comparison within the Annelida and the Lophotrochozoa. Despite having two developmental modes, there is no evidence of genome duplication or substantial gene number expansions. Instead, lineage specific repeats account for much of the expansion of this genome compared to other annelids.

genomics↗

bioRxiv2020

Baby makes three: maternal, paternal, and zygotic genetic effects shape larval phenotypic evolution

The evolutionary potential of a population is shaped by the genetic architecture of its life-history traits. Early-life phenotypes are influenced by both maternal and offspring genotype, and efforts to understand life-history evolution therefore require consideration of the interactions between these separate but correlated genomes. We used a four-generation experimental pedigree to estimate the genetic architecture of early-life phenotypes in a species with dramatic variation in larval size and morphology. In the polychaete annelid Streblospio benedicti, females make either many small eggs that develop into complex larvae that feed in the plankton or few large eggs that develop into benthic juveniles without having to feed as larvae. By isolating the contributions of maternal, paternal, and zygotic genotype to larval traits, we determined that larval anatomical structures are governed by the offspring genotype at a small number of large-effect loci. Larval size is not shaped by the larvas own genotype but instead depends on loci that act in the mother, and at two genomic locations, by loci that act in the father. The overall phenotype of each larva thus depends on three separate genomes, and a populations response to selection on larval traits will reflect the interactions among them.

evolutionary biology↗

bioRxiv2017

Decoupled Maternal and Zygotic Genetic Effects Shape the Evolution of Development

Many animals develop indirectly via a larval stage that is morphologically and ecologically distinct from its adult form. Hundreds of lineages across animal phylogeny have secondarily lost larval forms, instead producing offspring that directly develop into adult form without a distinct larval ecological niche1-7. Indirect development in the sea is typically planktotrophic: females produce large numbers of small offspring that require exogenous planktonic food to develop before metamorphosing into benthic juveniles. Direct development is typically lecithotrophic: females produce a smaller number of larger eggs, each developing into a juvenile without the need for larval feeding, provisioned by yolk. Evolutionary theory suggests that these alternative developmental strategies represent stable alternative fitness peaks, while intermediate states are disfavored4,8-11. Transitions from planktotrophy to lecithotrophy thus require crossing a fitness valley and represent radical and coordinated transformations of life-history, fecundity, ecology, dispersal, and development7,12-16. Here we dissect this transition in Streblospio benedicti, the sole genetically tractable species that harbors both states as heritable variation17-19. We identify large-effect loci that act maternally to influence larval size and independent, unlinked large-effect loci that act zygotically to affect discrete aspects of larval morphology. Because lecithotrophs and planktotrophs differ in both size and morphology, the genetic basis of larval form exhibits strong maternal-by-zygotic epistasis for fitness20. The fitness of zygotic alleles depends on their maternal background, creating a positive frequency-dependence that may homogenize local populations. Developmental and population genetics interact to shape larval evolution.

evolutionary biology↗