@article{harry_zakas_2024, title={The role of heterochronic gene expression and regulatory architecture in early developmental divergence}, url={https://doi.org/10.7554/eLife.93062.1}, DOI={10.7554/eLife.93062.1}, abstractNote={New developmental programs can evolve through adaptive changes to gene expression. The annelid S. 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 F 1 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. }, journal={eLife}, author={Harry, Nathan D. and Zakas, Christina}, year={2024}, month={Jan} } @article{ruskie_zakas_2023, title={Assortative mating and mate-choice contributes to the maintenance of a developmental dimorphism in Streblospio benedicti}, volume={5}, ISSN={["1552-5015"]}, url={https://doi.org/10.1002/jez.b.23196}, DOI={10.1002/jez.b.23196}, abstractNote={Abstract}, journal={JOURNAL OF EXPERIMENTAL ZOOLOGY PART B-MOLECULAR AND DEVELOPMENTAL EVOLUTION}, author={Ruskie, Erika L. and Zakas, Christina}, year={2023}, month={May} } @article{aguilar-camacho_harry_zakas_2023, title={Comparative Hox genes expression within the dimorphic annelidStreblospio benedictireveals patterning variation during development}, url={https://doi.org/10.1101/2023.12.20.572624}, DOI={10.1101/2023.12.20.572624}, abstractNote={ABSTRACT}, author={Aguilar-Camacho, Jose Maria and Harry, Nathan D. and Zakas, Christina}, year={2023}, month={Dec} } @article{zakas_martin-duran_2023, title={Genomics of Marine Larval Evolution and Development}, volume={8}, ISSN={["1557-7023"]}, url={https://doi.org/10.1093/icb/icad108}, DOI={10.1093/icb/icad108}, abstractNote={Synopsis}, journal={INTEGRATIVE AND COMPARATIVE BIOLOGY}, author={Zakas, Christina and Martin-Duran, Jose M.}, year={2023}, month={Aug} } @article{harry_zakas_2023, title={Maternal patterns of inheritance alter transcript expression in eggs}, volume={24}, ISSN={["1471-2164"]}, DOI={10.1186/s12864-023-09291-8}, abstractNote={Abstract}, number={1}, journal={BMC GENOMICS}, author={Harry, Nathan D. D. and Zakas, Christina}, year={2023}, month={Apr} } @article{harry_zakas_2023, title={The role of heterochronic gene expression and regulatory architecture in early developmental divergence}, url={https://doi.org/10.1101/2023.08.18.553877}, DOI={10.1101/2023.08.18.553877}, abstractNote={ABSTRACT}, author={Harry, Nathan D. and Zakas, Christina}, year={2023}, month={Aug} } @article{zakas_2022, title={Streblospio benedicti: A genetic model for understanding the evolution of development and life-history}, volume={147}, ISSN={["0070-2153"]}, DOI={10.1016/bs.ctdb.2021.12.021}, abstractNote={Investigating developmental evolution usually requires comparing differences across related species to infer how phenotypic change results from embryological modifications. However, when comparing organisms from different environments, ecologies, and evolutionary histories there can be many confounding factors to finding a genetic basis for developmental differences. In the marine annelid Streblospio benedicti, there are two distinct types of offspring with independent developmental pathways that converge on the same adult phenotype. To my knowledge, S. benedicti is the only known species that has heritable (additive) genetic variation in developmental traits that results in alternative life-history strategies. Females produce either hundreds of small, swimming and feeding larvae, or dozens of large, nonfeeding larvae. The larvae differ in their morphology, ecology, and dispersal potential. This developmental dimorphism makes S. benedicti a unique and useful model for understanding how genetic changes result in developmental modifications that ultimately lead to overall life-history differences. Because the offspring phenotypes of S. benedicti are heritable, we can use forward genetics within a single evolutionary lineage to disentangle how development evolves, and which genes and regulatory mechanisms are involved.}, journal={EMERGING MODEL SYSTEMS IN DEVELOPMENTAL BIOLOGY}, author={Zakas, Christina}, year={2022}, pages={496–520} } @article{zakas_harry_scholl_rockman_2022, title={The Genome of the Poecilogonous Annelid Streblospio benedicti}, volume={14}, ISSN={["1759-6653"]}, url={https://doi.org/10.1093/gbe/evac008}, DOI={10.1093/gbe/evac008}, abstractNote={Abstract}, number={2}, journal={GENOME BIOLOGY AND EVOLUTION}, author={Zakas, Christina and Harry, Nathan D. and Scholl, Elizabeth H. and Rockman, Matthew V}, editor={Lavrov, DennisEditor}, year={2022}, month={Feb} } @article{zakas_rockman_2021, title={Baby makes three: Maternal, paternal, and zygotic genetic effects shape larval phenotypic evolution}, volume={75}, ISSN={["1558-5646"]}, url={https://doi.org/10.1111/evo.14244}, DOI={10.1111/evo.14244}, abstractNote={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 larva’s 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 population’s response to selection on larval traits will reflect the interactions among them.}, number={7}, journal={EVOLUTION}, publisher={Wiley}, author={Zakas, Christina and Rockman, Matthew V.}, year={2021}, month={Jun} } @article{zakas_harry_scholl_rockman_2021, title={The genome of the poecilogonous annelid Streblospio benedicti}, volume={4}, url={https://doi.org/10.1101/2021.04.15.440069}, DOI={10.1101/2021.04.15.440069}, abstractNote={Abstract}, publisher={Cold Spring Harbor Laboratory}, author={Zakas, Christina and Harry, Nathan D. and Scholl, Elizabeth H. and Rockman, Matthew V.}, year={2021}, month={Apr} } @article{zakas_rockman_2020, title={Baby makes three: maternal, paternal, and zygotic genetic effects shape larval phenotypic evolution}, volume={12}, url={https://doi.org/10.1101/2020.12.10.419838}, DOI={10.1101/2020.12.10.419838}, abstractNote={ABSTRACT}, publisher={Cold Spring Harbor Laboratory}, author={Zakas, Christina and Rockman, Matthew V.}, year={2020}, month={Dec} } @article{zakas_deutscher_kay_rockman_2018, title={Decoupled maternal and zygotic genetic effects shape the evolution of development}, volume={7}, ISSN={2050-084X}, url={http://dx.doi.org/10.7554/elife.37143}, DOI={10.7554/elife.37143}, abstractNote={Evolutionary transitions from indirect to direct development involve changes in both maternal and zygotic genetic factors, with distinctive population-genetic implications, but empirical data on the genetics of such transitions are lacking. The polychaete Streblospio benedicti provides an opportunity to dissect a major transition in developmental mode using forward genetics. Females in this species produce either small eggs that develop into planktonic larvae or large eggs that develop into benthic juveniles. 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. The likely 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.}, journal={eLife}, publisher={eLife Sciences Publications, Ltd}, author={Zakas, Christina and Deutscher, Jennifer M and Kay, Alex D and Rockman, Matthew V}, year={2018}, month={Sep} } @article{zakas_rockman_2015, title={Gene-based polymorphisms reveal limited genomic divergence in a species with a heritable life-history dimorphism}, volume={17}, ISSN={1520-541X}, url={http://dx.doi.org/10.1111/ede.12128}, DOI={10.1111/ede.12128}, abstractNote={SUMMARY}, number={4}, journal={Evolution & Development}, publisher={Wiley}, author={Zakas, Christina and Rockman, Matthew V.}, year={2015}, month={Jul}, pages={240–247} } @article{zakas_rockman_2014, title={Dimorphic development in Streblospio benedicti: genetic analysis of morphological differences between larval types}, volume={58}, ISSN={0214-6282}, url={http://dx.doi.org/10.1387/ijdb.140088mr}, DOI={10.1387/ijdb.140088mr}, abstractNote={The marine polychaete Streblospio benedicti exhibits two distinct larval types, making it a model for the study of developmental evolution. Females produce either large eggs or small ones, which develop into distinct lecithotrophic or planktotrophic larvae with concomitant morphological and life-history differences. Here, we investigate the inheritance of key morphological traits that distinguish the larval types. We used genetic crosses to establish the influence of maternal and zygotic differences on larval phenotypes. We found a large maternal effect on larval size and the number of larval chaetae, while the number and length of these chaetae were also strongly influenced by zygotic genotype. Interestingly, the distribution of larval phenotypes produced by these crosses suggests traits intermediate to the two parental types should not be uncommon. Yet, despite gene flow between the types in natural populations, such intermediates are rarely found in nature, suggesting that selection may be maintaining distinct larval modes.}, number={6-7-8}, journal={The International Journal of Developmental Biology}, publisher={UPV/EHU Press}, author={Zakas, Christina and Rockman, Matthew V.}, year={2014}, pages={593–599} } @article{zakas_jones_wares_2013, title={Homogeneous Nuclear Background for Mitochondrial Cline in Northern Range of Notochthamalus scabrosus}, volume={4}, ISSN={2160-1836}, url={http://dx.doi.org/10.1534/g3.113.008383}, DOI={10.1534/g3.113.008383}, abstractNote={Abstract}, number={2}, journal={G3: Genes|Genomes|Genetics}, publisher={Genetics Society of America}, author={Zakas, Christina and Jones, Ken and Wares, John P.}, year={2013}, month={Dec}, pages={225–230} } @article{zakas_hall_2012, title={Asymmetric Dispersal Can Maintain Larval Polymorphism: A Model Motivated by Streblospio benedicti}, volume={52}, ISSN={1557-7023 1540-7063}, url={http://dx.doi.org/10.1093/icb/ics055}, DOI={10.1093/icb/ics055}, abstractNote={Polymorphism in traits affecting dispersal occurs in a diverse variety of taxa. Typically, the maintenance of a dispersal polymorphism is attributed to environmental heterogeneity where parental bet-hedging can be favored. There are, however, examples of dispersal polymorphisms that occur across similar environments. For example, the estuarine polychaete Streblospio benedicti has a highly heritable offspring dimorphism that affects larval dispersal potential. We use analytical models of dispersal to determine the conditions necessary for a stable dispersal polymorphism to exist. We show that in asexual haploids, sexual haploids, and in sexual diploids in the absence of overdominance, asymmetric dispersal is required in order to maintain a dispersal polymorphism when patches do not vary in intrinsic quality. Our study adds an additional factor, dispersal asymmetry, to the short list of mechanisms that can maintain polymorphism in nature. The region of the parameter space in which polymorphism is possible is limited, suggesting why dispersal polymorphisms within species are rare.}, number={1}, journal={Integrative and Comparative Biology}, publisher={Oxford University Press (OUP)}, author={Zakas, Christina and Hall, David W.}, year={2012}, month={May}, pages={197–212} } @article{zakas_wares_2012, title={Consequences of a poecilogonous life history for genetic structure in coastal populations of the polychaete Streblospio benedicti}, volume={21}, ISSN={0962-1083}, url={http://dx.doi.org/10.1111/mec.12040}, DOI={10.1111/mec.12040}, abstractNote={Abstract}, number={22}, journal={Molecular Ecology}, publisher={Wiley}, author={Zakas, Christina and Wares, John P.}, year={2012}, month={Oct}, pages={5447–5460} } @article{zakas_schult_mchugh_jones_wares_2012, title={Transcriptome Analysis and SNP Development Can Resolve Population Differentiation of Streblospio benedicti, a Developmentally Dimorphic Marine Annelid}, volume={7}, ISSN={1932-6203}, url={http://dx.doi.org/10.1371/journal.pone.0031613}, DOI={10.1371/journal.pone.0031613}, abstractNote={Next-generation sequencing technology is now frequently being used to develop genomic tools for non-model organisms, which are generally important for advancing studies of evolutionary ecology. One such species, the marine annelid Streblospio benedicti, is an ideal system to study the evolutionary consequences of larval life history mode because the species displays a rare offspring dimorphism termed poecilogony, where females can produce either many small offspring or a few large ones. To further develop S. benedicti as a model system for studies of life history evolution, we apply 454 sequencing to characterize the transcriptome for embryos, larvae, and juveniles of this species, for which no genomic resources are currently available. Here we performed a de novo alignment of 336,715 reads generated by a quarter GS-FLX (Roche 454) run, which produced 7,222 contigs. We developed a novel approach for evaluating the site frequency spectrum across the transcriptome to identify potential signatures of selection. We also developed 84 novel single nucleotide polymorphism (SNP) markers for this species that are used to distinguish coastal populations of S. benedicti. We validated the SNPs by genotyping individuals of different developmental modes using the BeadXPress Golden Gate assay (Illumina). This allowed us to evaluate markers that may be associated with life-history mode.}, number={2}, journal={PLoS ONE}, publisher={Public Library of Science (PLoS)}, author={Zakas, Christina and Schult, Nancy and McHugh, Damhnait and Jones, Kenneth L. and Wares, John P.}, editor={Zwick, Michael EdwardEditor}, year={2012}, month={Feb}, pages={e31613} } @article{zakas_binford_navarrete_wares_2009, title={Restricted gene flow in Chilean barnacles reflects an oceanographic and biogeographic transition zone}, volume={394}, ISSN={0171-8630 1616-1599}, url={http://dx.doi.org/10.3354/meps08265}, DOI={10.3354/meps08265}, abstractNote={Broad scale patterns of genetic structure in coastal communities are strongly affected by both ecological transitions and larval dispersal. Along the Chilean coast, we examined 2 species of co-distributed barnacles, Jehlius cirratus and Notochthamalus scabrosus, which span an ecological transition associated with a sharp increase in larval recruitment. A distinct break in haplotype fre- quencies in the mitochondrial cytochrome oxidase I (mtCOI) gene was detected in N. scabrosus, with only marginal genetic structure observed in J. cirratus, suggesting significant differences in either selective pressures or dispersal ability between the species. The nuclear gene elongation factor 1α was also analyzed in N. scabrosus, and similarly suggested limited gene flow. The sharp genetic tran- sition is downstream of the described ecological transition, effectively mirroring a genetic cline described in a different barnacle species along the North American Pacific coast.}, journal={Marine Ecology Progress Series}, publisher={Inter-Research Science Center}, author={Zakas, C and Binford, J and Navarrete, SA and Wares, JP}, year={2009}, month={Nov}, pages={165–177} } @article{allen_zakas_podolsky_2006, title={Effects of egg size reduction and larval feeding on juvenile quality for a species with facultative-feeding development}, volume={331}, ISSN={0022-0981}, url={http://dx.doi.org/10.1016/j.jembe.2005.10.020}, DOI={10.1016/j.jembe.2005.10.020}, abstractNote={In free-spawning marine invertebrates, larval development typically proceeds by one of two modes: planktotrophy (obligate larval feeding) from small eggs or lecithotrophy (obligate non-feeding) from relatively large eggs. In a rare third developmental mode, facultative planktotrophy, larvae can feed, but do not require particulate food to complete metamorphosis. Facultative planktotrophy is thought to be an intermediate condition that results from an evolutionary increase in energy content in the small eggs of a planktotrophic ancestor. We tested whether an experimental reduction in egg size is sufficient to restore obligate planktotrophy from facultative planktotrophy and whether the two sources of larval nutrition (feeding and energy in the egg) differentially influence larval survival and juvenile quality. We predicted, based on its large egg size, that a reduction in egg size in the echinoid echinoderm Clypeaster rosaceus would affect juvenile size but not time to metamorphosis. We reduced the effective size of whole (W) zygotes by separating blastomeres at the two- or four-cell stages to create half- (H) or quarter-size (Q) "zygotes" and reared larvae to metamorphosis, both with and without particulate food. Larvae metamorphosed at approximately the same time regardless of food or egg size treatment. In contrast, juveniles that developed from W zygotes were significantly larger, had higher organic content and had longer and more numerous spines than juveniles from H or Q zygotes. Larvae from W, H and Q zygotes were able to reach metamorphosis without feeding, suggesting that the evolution of facultative planktotrophy in C. rosaceus was accompanied by more than a simple increase in egg size. In addition, our results suggest that resources lost by halving egg size have a larger effect on larval survival and juvenile quality than those lost by withholding particulate food.}, number={2}, journal={Journal of Experimental Marine Biology and Ecology}, publisher={Elsevier BV}, author={Allen, Jonathan D. and Zakas, Christina and Podolsky, Robert D.}, year={2006}, month={Apr}, pages={186–197} }