Whitehead Andrew

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  • Article
    The landscape of extreme genomic variation in the highly adaptable Atlantic killifish
    (Oxford University Press, 2017-03-01) Reid, Noah M. ; Jackson, Craig E. ; Gilbert, Don ; Minx, Patrick ; Montague, Michael J. ; Hampton, Thomas H. ; Helfrich, Lily W. ; King, Benjamin L. ; Nacci, Diane E. ; Aluru, Neelakanteswar ; Karchner, Sibel I. ; Colbourne, John K. ; Hahn, Mark E. ; Shaw, Joseph R. ; Oleksiak, Marjorie F. ; Crawford, Douglas L. ; Warren, Wesley C. ; Whitehead, Andrew
    Understanding and predicting the fate of populations in changing environments require knowledge about the mechanisms that support phenotypic plasticity and the adaptive value and evolutionary fate of genetic variation within populations. Atlantic killifish (Fundulus heteroclitus) exhibit extensive phenotypic plasticity that supports large population sizes in highly fluctuating estuarine environments. Populations have also evolved diverse local adaptations. To yield insights into the genomic variation that supports their adaptability, we sequenced a reference genome and 48 additional whole genomes from a wild population. Evolution of genes associated with cell cycle regulation and apoptosis is accelerated along the killifish lineage, which is likely tied to adaptations for life in highly variable estuarine environments. Genome-wide standing genetic variation, including nucleotide diversity and copy number variation, is extremely high. The highest diversity genes are those associated with immune function and olfaction, whereas genes under greatest evolutionary constraint are those associated with neurological, developmental, and cytoskeletal functions. Reduced genetic variation is detected for tight junction proteins, which in killifish regulate paracellular permeability that supports their extreme physiological flexibility. Low-diversity genes engage in more regulatory interactions than high-diversity genes, consistent with the influence of pleiotropic constraint on molecular evolution. High genetic variation is crucial for continued persistence of species given the pace of contemporary environmental change. Killifish populations harbor among the highest levels of nucleotide diversity yet reported for a vertebrate species, and thus may serve as a useful model system for studying evolutionary potential in variable and changing environments.
  • Article
    When evolution is the solution to pollution : key principles, and lessons from rapid repeated adaptation of killifish (Fundulus heteroclitus) populations
    (John Wiley & Sons, 2017-04-26) Whitehead, Andrew ; Clark, Bryan W. ; Reid, Noah M. ; Hahn, Mark E. ; Nacci, Diane E.
    For most species, evolutionary adaptation is not expected to be sufficiently rapid to buffer the effects of human-mediated environmental changes, including environmental pollution. Here we review how key features of populations, the characteristics of environmental pollution, and the genetic architecture underlying adaptive traits, may interact to shape the likelihood of evolutionary rescue from pollution. Large populations of Atlantic killifish (Fundulus heteroclitus) persist in some of the most contaminated estuaries of the United States, and killifish studies have provided some of the first insights into the types of genomic changes that enable rapid evolutionary rescue from complexly degraded environments. We describe how selection by industrial pollutants and other stressors has acted on multiple populations of killifish and posit that extreme nucleotide diversity uniquely positions this species for successful evolutionary adaptation. Mechanistic studies have identified some of the genetic underpinnings of adaptation to a well-studied class of toxic pollutants; however, multiple genetic regions under selection in wild populations seem to reflect more complex responses to diverse native stressors and/or compensatory responses to primary adaptation. The discovery of these pollution-adapted killifish populations suggests that the evolutionary influence of anthropogenic stressors as selective agents occurs widely. Yet adaptation to chemical pollution in terrestrial and aquatic vertebrate wildlife may rarely be a successful “solution to pollution” because potentially adaptive phenotypes may be complex and incur fitness costs, and therefore be unlikely to evolve quickly enough, especially in species with small population sizes.
  • Preprint
    Fundulus as the premier teleost model in environmental biology : opportunities for new insights using genomics
    ( 2007-09-01) Burnett, Karen G. ; Bain, Lisa J. ; Baldwin, William S. ; Callard, Gloria V. ; Cohen, Sarah ; Di Giulio, Richard T. ; Evans, David H. ; Gomez-Chiarri, Marta ; Hahn, Mark E. ; Hoover, Cindi A. ; Karchner, Sibel I. ; Katoh, Fumi ; MacLatchy, Deborah L. ; Marshall, William S. ; Meyer, Joel N. ; Nacci, Diane E. ; Oleksiak, Marjorie F. ; Rees, Bernard B. ; Singer, Thomas D. ; Stegeman, John J. ; Towle, David W. ; Van Veld, Peter A. ; Vogelbein, Wolfgang K. ; Whitehead, Andrew ; Winn, Richard N. ; Crawford, Douglas L.
    A strong foundation of basic and applied research documents that the estuarine fish Fundulus heteroclitus and related species are unique laboratory and field models for understanding how individuals and populations interact with their environment. In this paper we summarize an extensive body of work examining the adaptive responses of Fundulus species to environmental conditions, and describe how this research has contributed importantly to our understanding of physiology, gene regulation, toxicology, and ecological and evolutionary genetics of teleosts and other vertebrates. These explorations have reached a critical juncture at which advancement is hindered by the lack of genomic resources for these species. We suggest that a more complete genomics toolbox for F. heteroclitus and related species will permit researchers to exploit the power of this model organism to rapidly advance our understanding of fundamental biological and pathological mechanisms among vertebrates, as well as ecological strategies and evolutionary processes common to all living organisms.
  • Preprint
    The genomic landscape of rapid repeated evolutionary adaptation to toxic pollution in wild fish
    ( 2016-10) Reid, Noah M. ; Proestou, Dina A. ; Clark, Bryan W. ; Warren, Wesley C. ; Colbourne, John K. ; Shaw, Joseph R. ; Karchner, Sibel I. ; Hahn, Mark E. ; Nacci, Diane E. ; Oleksiak, Marjorie F. ; Crawford, Douglas L. ; Whitehead, Andrew
    Atlantic killifish populations have rapidly adapted to normally lethal levels of pollution in four urban estuaries. Through analysis of 384 whole killifish genome sequences and comparative transcriptomics in four pairs of sensitive and tolerant populations, we identify the aryl hydrocarbon receptor-based signaling pathway as a shared target of selection. This suggests evolutionary constraint on adaptive solutions to complex toxicant mixtures at each site. However, distinct molecular variants apparently contribute to adaptive pathway modification among tolerant populations. Selection also targets other toxicity-mediating genes, and genes of connected signaling pathways, indicating complex tolerance phenotypes and potentially compensatory adaptations. Molecular changes are consistent with selection on standing genetic variation. In killifish high nucleotide diversity has likely been a crucial substrate for selective sweeps to propel rapid adaptation.
  • Preprint
    Ryanodine receptor and FK506 binding protein 1 in the Atlantic killifish (Fundulus heteroclitus) : a phylogenetic and population-based comparison
    ( 2017-09) Holland, Erika B. ; Goldstone, Jared V. ; Pessah, Isaac N. ; Whitehead, Andrew ; Reid, Noah M. ; Karchner, Sibel I. ; Hahn, Mark E. ; Nacci, Diane E. ; Clark, Bryan W. ; Stegeman, John J.
    Non-dioxin-like polychlorinated biphenyls (NDL PCBs) activate ryanodine receptors (RyR), microsomal Ca2+ channels of broad significance. Teleost fish may be important models for NDL PCB neurotoxicity, and we used sequencing databases to characterize teleost RyR and FK506 binding protein 12 or 12.6 kDa (genes FKBP1A; FKBP1B), which promote NDL PCB-triggered Ca2+ dysregulation. Particular focus was placed on describing genes in the Atlantic killifish (Fundulus heteroclitus) genome and searching available RNA-sequencing datasets for single nucleotide variants (SNV) between PCB tolerant killifish from New Bedford Harbor (NBH) versus sensitive killifish from Scorton Creek (SC), MA. Consistent with the teleost whole genome duplication (tWGD), killifish have six RyR genes, corresponding to a and b paralogs of mammalian RyR1, 2 and 3. The presence of six RyR genes was consistent in all teleosts investigated including zebrafish. Killifish have four FKBP1; one FKBP1b and three FKBP1a named FKBP1aa, FKBP1ab, likely from the tWGD and a single gene duplicate FKBP1a3 suggested to have arisen in Atherinomorphae. The RyR and FKBP1 genes displayed tissue and developmental stage-specific mRNA expression, and the previously uncharacterized RyR3, herein named RyR3b, and all FKBP1 genes were prominent in brain. We identified a SNV in RyR3b encoding missense mutation E1458D. In NBH killifish, 57% were heterozygous and 28% were homozygous for this SNV, whereas almost all SC killifish (94%) lacked the variant (n≥39 per population). The outlined sequence differences between mammalian and teleost RyR and FKBP1 together with outlined population differences in SNV frequency may contribute to our understanding of NDL PCB neurotoxicity.
  • Article
    Independently evolved pollution resistance in four killifish populations is largely explained by few variants of large effect
    (Wiley, 2024-01-29) Miller, Jeffrey T. ; Clark, Bryan W. ; Reid, Noah M. ; Karchner, Sibel I. ; Roach, Jennifer L. ; Hahn, Mark E. ; Nacci, Diane E. ; Whitehead, Andrew
    The genetic architecture of phenotypic traits can affect the mode and tempo of trait evolution. Human-altered environments can impose strong natural selection, where successful evolutionary adaptation requires swift and large phenotypic shifts. In these scenarios, theory predicts that adaptation is due to a few adaptive variants of large effect, but empirical studies that have revealed the genetic architecture of rapidly evolved phenotypes are rare, especially for populations inhabiting polluted environments. Fundulus killifish have repeatedly evolved adaptive resistance to extreme pollution in urban estuaries. Prior studies, including genome scans for signatures of natural selection, have revealed some of the genes and pathways important for evolved pollution resistance, and provide context for the genotype–phenotype association studies reported here. We created multiple quantitative trait locus (QTL) mapping families using progenitors from four different resistant populations, and using RAD-seq genetically mapped variation in sensitivity (developmental perturbations) following embryonic exposure to a model toxicant PCB-126. We found that one to two large-effect QTL loci accounted for resistance to PCB-mediated developmental toxicity. QTLs harbored candidate genes that govern the regulation of aryl hydrocarbon receptor (AHR) signaling. One QTL locus was shared across all populations and another was shared across three populations. One QTL locus showed strong signatures of recent natural selection in the corresponding wild population but another QTL locus did not. Some candidate genes for PCB resistance inferred from genome scans in wild populations were identified as QTL, but some key candidate genes were not. We conclude that rapidly evolved resistance to the developmental defects normally caused by PCB-126 is governed by few genes of large effect. However, other aspects of resistance beyond developmental phenotypes may be governed by additional loci, such that comprehensive resistance to PCB-126, and to the mixtures of chemicals that distinguish urban estuaries more broadly, may be more genetically complex.