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Logsdon, J. M.

Publications and source records attributed to Logsdon, J. M..

8 recordsLinked to original sources

Losses of TMC and CIB neurosensory genes in schizophoran flies at the PETM

The K-Pg extinction ended the world of non-avian dinosaurs 66 Mya and ushered in the Age of Mammals. During the [~]10 My of recovery, Schizophora, an immensely successful group of flies, appeared, flourished and diversified. This large radiation produced over half of all dipteran families ([~]78/150), including the family for Drosophila, the model genetic powerhouse. In the context of this evolutionary radiation, we investigate the loss of two of three highly conserved, neurosensory transmembrane channel (TMC) genes. Here, we show that these genes were separately lost across multiple diverging schizophoran lineages of the early Paleogene, suggesting a powerful environmental driver was involved. We also show that unlinked genes encoding the calcium- and integrin-binding (CIB) subunits of the missing TMC complexes were lost during the same time frame. Because the lost genes encode complexes involved in thermal nociception, we propose the external driver was likely the Paleocene- Eocene thermal maximum (PETM), a 200 ky interval of elevated global temperatures occurring 56 Mya, slightly before the earliest schizophoran fossil from 53 Mya. These results suggest that gene loss may have been adaptive for most schizophoran lineages to emerge past the hothouse Earth of the PETM.

evolutionary biology↗

Whole-genome sequence of Potamopyrgus antipodarum: a model system for the maintenance of sexual reproduction reveals a recent whole-genome duplication

Key unanswered questions in biology center on the causes, consequences, and maintenance of sexual reproduction ("sex"). Genome-driven processes are central to the evolutionary and genetic mechanisms inherent to sex, making genomic resources a fundamental part of answering these questions. We present the first genome assembly for a species that is uniquely well-suited for the study of (a)sex in nature, Potamopyrgus antipodarum. This New Zealand snail is unusual in featuring multiple separate transitions from obligately sexual to obligately asexual reproduction, leading to the coexistence of phenotypically similar sexual and asexual forms, a feature that is required to directly study the maintenance of sex. These separately derived asexual lineages constitute separate evolutionary experiments, providing a powerful means of characterizing how the absence of sex affects genome evolution. Our genome assembly provides critical steps towards understanding causes and consequences of sex in this system and important resources for the rapidly growing P. antipodarum and molluscan genomics research community. In characterizing this genome, we uncovered unexpected evidence for a recent whole-genome duplication (WGD) in P. antipodarum. This discovery sets the stage for using P. antipodarum to evaluate processes of rediploidization following WGD and assess whether WGD might drive transitions to asexuality.

genomics↗

Genome evolution and introgression in the New Zealand mud snails Potamopyrgus estuarinus and Potamopyrgus kaitunuparaoa

We have sequenced, assembled, and analyzed the nuclear and mitochondrial genomes and transcriptomes of Potamopyrgus estuarinus and Potamopyrgus kaitunuparaoa, two prosobranch snail species native to New Zealand that together span the continuum from estuary to freshwater. These two species are the closest known relatives of the freshwater species P. antipodarum--a model for studying the evolution of sex, host-parasite coevolution, and biological invasiveness--and thus provide key evolutionary context for understanding its unusual biology. The P. estuarinus and P. kaitunuparaoa genomes are very similar in size and overall gene content. Comparative analyses of genome content indicate that these two species harbor a near-identical set of genes involved in meiosis and sperm functions, including seven genes with meiosis-specific functions. These results are consistent with obligate sexual reproduction in these two species and provide a framework for future analyses of P. antipodarum--a species comprising both obligately sexual and obligately asexual lineages, each separately derived from a sexual ancestor. Genome-wide multigene phylogenetic analyses indicate that P. kaitunuparaoa is likely the closest relative to P. antipodarum. We nevertheless show that there has been considerable introgression between P. estuarinus and P. kaitunuparaoa. That introgression does not extend to the mitochondrial genome, which appears to serve as a barrier to hybridization between P. estuarinus and P. kaitunuparaoa. Nuclear-encoded genes whose products function in joint mitochondrial-nuclear enzyme complexes exhibit similar patterns of non-introgression, indicating that incompatibilities between the mitochondrial and the nuclear genome may have prevented more extensive gene flow between these two species. Significance StatementNo whole-nuclear genome sequences are currently available for snails of the genus Potamopyrgus, best known for Potamopyrgus antipodarum, an invasive species of rivers and lakes worldwide, and a famous model for the study of the evolution of sex. We have sequenced and analyzed the genome of sexual P. estuarinus and P. kaitunuparaoa, the closest known relatives of P. antipodarum. We show that 1) the genomes are very similar in gene content and size, 2) P. kaitunuparaoa is the closest relative to P. antipodarum, 3) significant introgression has occurred between P. estuarinus and P. kaitunuparaoa; these genomes set the stage for powerful direct analyses of the genomic features, e.g., sex to asexual transitions and invasive success, that make P. antipodarum unique.

evolutionary biology↗

Single-molecule sequencing of animal mitochondrial genomes reveals chloroplast-like architecture and repeat-mediated recombination

Recent advances in long-read sequencing technology have allowed for single-molecule sequencing of entire mitochondrial genomes, opening the door for direct investigation of mitochondrial genome architecture and landscapes of recombination. We used PacBio sequencing to re-assemble mitochondrial genomes from two species of New Zealand freshwater snails, Potamopyrgus antipodarum and Potamopyrgus estuarinus. These assemblies revealed a [~]1.7 kb structure within the mitochondrial genomes of both species that was previously undetected by assembly of short sequencing reads and likely corresponding to a large non-coding region commonly present in mitochondrial genomes. The overall architecture of these Potamopyrgus mitochondrial genomes is reminiscent of the chloroplast genomes of land plants, harboring a large single-copy region (LSC) and a small single-copy region (SSC) separated by a pair of inverted repeats (IRa and IRb). Individual sequencing reads that spanned across the Potamopyrgus IRa-SSC-IRb structure revealed the occurrence of "flip-flop" recombination, apparently mediated by the IRs. We also detected evidence for two distinct IR haplotypes and recombination between them in wild-caught P. estuarinus, as well as extensive inter-molecular recombination between SNPs in the LSC region. Together, these observations suggest that mitochondrial inheritance is not strictly maternal in these snails. The chloroplast-like architecture and repeat-mediated mitochondrial recombination we describe here raise fundamental questions regarding the origins and commonness of such architecture, whether and how recombination mediates mitochondrial genome evolution, and the role of genome architecture in driving cytoplasmic genome biology and the maintenance of cytoplasmic genomes.

evolutionary biology↗

Genome evolution in a putatively asexual wasp

Asexual lineages are destined for extinction--a result predicted by theory and revealed in practice. Short-term benefits of asexuality are eventually outstripped by their fitness costs: losses of sex and recombination are together expected to reduce efficacy of selection, increase mutation load, and thus, lower fitness. We characterized genomic patterns of accumulating mutations in Diachasma muliebre, a parasitic wasp that has apparently lost sex, an inference supported by many decades of field collections of 1000s of individuals in which only females were found. The split between D. muliebre and its closest sexual relative, Diachasma ferrugineum, is quite recent, allowing us to observe initial events in the evolution of this putative asexual species. First, we find a faster rate of molecular evolution across the D. muliebre genome. In addition, we observed a marked excess of replacement nucleotide substitutions in orthologous genes in the putatively asexual D. muliebre when compared to D. ferrugineum. This pattern directly indicates genome-wide relaxed selection in this young, putatively asexual species, the resulting mutational load from which is expected to ultimately lead to extinction. However, these genomic effects occur in the presence of genomic recombination initially detected by a previous study and also supported by analyses of genome-wide substitution rates within codons. In addition, following completion of the genome sequence and its analysis, we discovered two D. muliebre males, suggesting the possibility of rare sex in this species. Haplodiploid animals, including the sexual ancestors of D. muliebre, bear small genetic loads, likely making their initial transitions to asexuality relatively benign. Paradoxically, an elevated rate of mutation accumulation resulting from asexuality, when accompanied by retention of recombination and/or rare sex, could actually be beneficial: we hypothesize that the novel variation introduced by mutation along with limited shuffling of genes may facilitate initial adaptation and extend persistence of such lineages.

evolutionary biology↗

Multiple separate cases of pseudogenized meiosis genes Msh4 and Msh5 in Eurotiomycete fungi: associations with Zip3 sequence evolution and homothallism, but not Pch2 losses

The overall process of meiosis is conserved in many species, including some lineages that have lost various ancestrally present meiosis genes. The extent to which individual meiosis gene losses are independent from or dependent on one another is largely unknown. Various Eurotiomycete fungi were investigated as a case system of recent meiosis gene losses after BLAST and synteny comparisons found Msh4, Msh5, Pch2, and Zip3 to be either pseudogenized or undetected in Aspergillus nidulans yet intact in congeners such as A. fumigatus. Flanking gene-targeted degenerate PCR primers applied to 9 additional Aspergillus species found (i) Msh4, Msh5, and Zip3 pseudogenized in A. rugulosus (sister taxon to A. nidulans) but intact in all other amplified sequences; and (ii) Pch2 not present at the syntenic locus in most of the 9 species. Topology tests suggested two independent Pch2 losses in genus Aspergillus, neither directly coinciding with pseudogenization of the other three genes. The A. nidulans-A. conjunctus clade Pch2 loss was not associated with significant Ka/Ks changes for Msh4, Msh5, or Zip3; this suggests against prior Pch2 loss directly altering sequence evolution constraints on these three genes. By contrast, Zip3 Ka/Ks tended to be elevated in several other Eurotiomycete fungi with independently pseudogenized Msh4 and Msh5 (Talaromyces stipitatus, Eurotium herbariorum). The coinciding Ka/Ks elevation and/or clear pseudogenization of Zip3 in taxa with pseudogenized Msh4 and Msh5 is consistent with some degree of molecular coevolution. Possible molecular, environmental, and life history variables (e.g., homothallism) that may be associated with these numerous independent meiosis gene losses (Msh4: 3, Msh5: 3, Zip3: [≥] 1, Pch2: 4) are discussed.

genetics↗

Male evolution under relaxed selection: Evidence for degeneration in sperm produced by male snails from asexual lineages

How drastic changes in selective regimes affect trait evolution is an important open biological question. We take advantage of naturally occurring and repeated transitions from sexual to asexual reproduction in a New Zealand freshwater snail species to address how relaxed selection on male-specific traits influences sperm morphology. The occasional production of male offspring by the otherwise all-female asexual lineages allows a unique and powerful opportunity to assess the fate of sperm traits in a context where males are unnecessary. These comparisons revealed that the sperm produced by "asexual" males are markedly distinct from sexual counterparts. In particular, the asexual male sperm harbored markedly higher phenotypic variation and was much more likely to be morphologically abnormal. Together, these data suggest that transitions to asexual reproduction might be irreversible at least in part because male function is likely to be compromised. More broadly, our results are consistent with a scenario where relaxed selection translates into rapid trait degeneration.

evolutionary biology↗

Genome of the parasitoid wasp Diachasma alloeum, an emerging model for ecological speciation and transitions to asexual reproduction

Parasitoid wasps are among the most speciose animals, yet have relatively few available genomic resources. We report a draft genome assembly of the wasp Diachasma alloeum (Hymenoptera: Braconidae), a host-specific parasitoid of the apple maggot fly Rhagoletis pomonella (Diptera: Tephritidae) and a developing model for understanding how ecological speciation can "cascade" across trophic levels. Identification of gene content confirmed the overall quality of the draft genome, and we manually annotated [~]400 genes as part of this study, including those involved in oxidative phosphorylation, chemosensation, and reproduction. Through comparisons to model hymenopterans such as the European honeybee Apis mellifera and parasitoid wasp Nasonia vitripennis, as well as a more closely related braconid parasitoid Microplitis demolitor, we identified a proliferation of transposable elements in the genome, an expansion of chemosensory genes in D. alloeum and other parasitoid wasps, and the maintenance of several key genes with known roles in sexual reproduction and sex determination. The D. alloeum genome will provide a valuable resource for comparative genomics studies in Hymenoptera as well as specific investigations into the genomic changes associated with ecological speciation and transitions to asexuality.

genomics↗