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Cooper, J. C.

Publications and source records attributed to Cooper, J. C..

10 recordsLinked to original sources

Hybrid Drosophila cell lines show selective genome instabilities

Background: Post-zygotic reproductive isolation is thought to be caused by genomic conflict. However, the exact nature of these detrimental incompatibilities is largely unknown. To identify genomic regions that became incompatible during the formation of species and are therefore prone to get lost in hybrids, we established hybrid cell lines derived from an authentic interspecies cross between Drosophila melanogaster and Drosophila simulans. Results: All four independently derived lines selectively lost the D. melanogaster allele of the hybrid incompatibility gene Hmr, confirming its incompatibility with cellular viability. Moreover, each line underwent distinct but directionally biased erosion of additional D. melanogaster chromosomal regions, preferentially affecting the X chromosome, chromosome 4, and chromosome 3R. Loss of the D. melanogaster X was dosage compensated by upregulation of genes on the hemizygous D. simulans X, while D. melanogaster rDNA was paradoxically amplified across all lines. Nucleolar dominance was driven by relative rDNA copy number rather than species identity, overturning the prevailing view of fixed species-based dominance. Finally, the measurements of the species-specific proteome revealed species specific differences in the RNA to protein coefficient K_p as novel and yet undescribed sources of molecular conflict in hybrids. Conclusions: These findings reveal a hierarchical, constraint-driven mechanism of hybrid genome resolution.

evolutionary biology↗

Overdrive is essential for targeted sperm elimination by Segregation Distorter

Intra-genomic conflict driven by selfish chromosomes is a powerful force that shapes the evolution of genomes and species. In the male germline, many selfish chromosomes bias transmission in their own favor by eliminating spermatids bearing the competing homologous chromosomes. However, the mechanisms of targeted gamete elimination remain mysterious. Here, we show that Overdrive (Ovd), a gene required for both segregation distortion and male sterility in Drosophila pseudoobscura hybrids, is broadly conserved in Dipteran insects but dispensable for viability and fertility. In D. melanogaster, Ovd is required for targeted Responder spermatid elimination after the histone-to-protamine transition in the classical Segregation Distorter system. We propose that Ovd functions as a general spermatid quality checkpoint that is hijacked by independent selfish chromosomes to eliminate competing gametes.

genetics↗

Ecological niche divergence or ecological niche partitioning in a widespread Neotropical bird lineage

Ecological niche divergence is generally considered to be a facet of evolution that may accompany geographic isolation and diversification in allopatry, contributing to species evolutionary distinctiveness through time. The null expectation for any two diverging species in geographic isolation is that of niche conservatism, wherein populations do not rapidly shift to or adapt to novel environments. Here, I test ecological niche divergence for a widespread, pan- American lineage, the avian genus of martins (Progne). Despite containing species with distributions that go from continent-spanning to locally endemic, I found limited evidence for niche divergence across the breeding distributions of Progne, and much stronger support for niche conservatism with patterns of niche partitioning. The ancestral Progne had a relatively broad ecological niche, similar to extant basal Progne lineages, and several geographically localized descendant species occupy only portions of the larger ancestral Progne niche. I recovered strong evidence of breeding niche divergence for four of 36 taxon pairs but only one of these divergent pairs involved two widespread, continental species (Southern Martin P. elegans vs. Gray-breasted Martin P. chalybea). Potential niche expansion from the ancestral species was observed in the most wide-ranging present-day species, namely the North American Purple Martin P. subis and P. chalybea. I analyzed populations of P. subis separately, as a microcosm of Progne evolution, and again found only limited evidence of niche divergence. This study adds to the mounting evidence for niche conservatism as a dominant feature of diversifying lineages. Even taxa that appear unique in terms of habitat or behavior may still not be diversifying with respect to their ecological niches, but merely partitioning ancestral niches among descendant taxa.

evolutionary biology↗

Testing the accuracy of species distribution models based on community science data

While traditional methods of tracking species, collecting specimens, and performing surveys are known to be accurate, additional opportunities to broaden the data pool are evolving. Community science data5 has emerged as a new way of gathering large amounts of data, but little research has been done on its reliability for making models for novel locations. The goal of this project was to test the reliability of eBird data as the primary dataset for ecological niche modeling by determining the accuracy of models derived from the citizen-science based eBird dataset. I made species distribution models of 676 bird species in Costa Rica based on eBird observations to predict which species would be found in two localities in Costa Rica that were surveyed. I compared the predictions with these field surveys to determine the prediction success and Sorensen index of the models. Overall, I found that while spatio-temporal factors can affect the accuracy of ecological models, eBird data have great potential as data for species distribution modeling. The models more accurately predicted the community composition in the rural locality as opposed to the more urban locality, and the accuracy of the models increased when compared with data that covered two month as opposed to one month time periods. I tested to see how the number of observations per species influenced the predictive ability of the models and determined that an intermediate number of observations led to better models. These are important metrics to understand because modeling can be an informative and cost effective way to monitor inaccessible areas and can be used in conservation efforts.

ecology↗

Is niche divergence more likely in parapatry? A test in Sclerurus mexicanus sensu lato (Aves: Furnariidae)

AimWhile species niches are understood to diverge through time, the mode of these divergences is not fully understood. The null hypothesis of niche divergence in the present is that of conservatism; that species are likely to occur in the same environment as their ancestors and, therefore, as allopatric sister species. Alternatively, species are expected to diverge when selective pressure, such as parapatry with a congener, occurs. Here, we analyse niche divergence in a mosaic of allo- and parapatric Sclerurus mexicanus sensu lato populations to determine if niche divergence is more likely in parapatry. LocationNeotropics. MethodsWe created a dataset of 1,100 vetted localities for S. mexicanus sensu lato, and assigned each point to each of the seven described populations. We created individual dispersal areas for each species in Maxent following: 1) a broad approach in which training areas where allowed to overlap with parapatric congeners; and 2) a narrow approach in which species dispersal areas adhered to strict parapatry and there was no overlap in training areas. We complemented these ENMs with random models drawn from points within each training area, thus creating null ENMs against which we could test niche divergence using the metric Schoeners D. ResultsThere was no significant difference in the performance of broad and narrow training areas. Few significant divergences were found, and all of those that were found consisted of allopatric populations. Partial divergences were frequently recovered when comparing parapatric taxa. Main conclusionsIn contrast to our expectation, we found no significant evidence for increased niche divergence in parapatric versus allopatric species. Possible explanations for these findings include true conservatism even among parapatric lineages (e.g., additional environmental or biological factors may delimit distributions) or artefactual errors inherent to model creation. We discuss the implications of these findings, and discuss ways to improve upon tests of niche divergence in the future, especially when dealing with cases of parapatry.

ecology↗

Endless Conflicts: Detecting Molecular Arms Races in Mammalian Genomes

Recurrent positive selection at the codon level is often a sign that a gene is engaged in a molecular arms race - a conflict between the genome of its host and the genome of another species over mutually exclusive access to a resource that has a direct effect on the fitness of both individuals. Detecting molecular arms races has led to a better understanding of how evolution changes the molecular interfaces of proteins when organisms compete over time, especially in the realm of host-pathogen interactions. Here, we present a method for detection of gene-level recurrent positive selection across entire genomes for a given phylogenetic group. We deploy this method on five mammalian clades - primates, mice, deer mice, dogs, and bats - to both detect novel instances of recurrent positive selection and to compare the prevalence of recurrent positive selection between clades. We analyze the frequency at which individual genes are targets of recurrent positive selection in multiple clades. We find that coincidence of selection occurs far more frequently than expected by chance, indicating that all clades experience shared selective pressures. Additionally, we highlight Polymeric Immunoglobulin Receptor (PIGR) as a gene which shares specific amino acids under recurrent positive selection in multiple clades, indicating that it has been locked in a molecular arms race for [~]100My. These data provide an in-depth comparison of recurrent positive selection across the mammalian phylogeny, and highlights of the power of comparative evolutionary approaches to generate specific hypotheses about the molecular interactions of rapidly evolving genes.

evolutionary biology↗

A triple-hybrid cross reveals new a hybrid incompatibility locus between D. melanogaster and D. sechellia

Hybrid incompatibilities are the result of deleterious interactions between diverged genes in the progeny of two species. In Drosophila, crosses between female D. melanogaster and males from the D. simulans clade (D. simulans, D. mauritiana, D. sechellia) fail to produce hybrid F1 males. When attempting to rescue hybrid F1 males by depleting the incompatible allele of a previously identified hybrid incompatibility gene, we observed robust rescue in crosses of D. melanogaster to D. simulans or D. mauritiana, but no rescue in crosses to D. sechellia. To investigate the genetic basis of D. sechellia resistance to hybrid rescue, we designed a triple-hybrid cross to generate recombinant D. sechellia / D. simulans genotypes. We tested the ability of those genotypes to rescue hybrid males with D. melanogaster, and used whole genome sequencing to measure the D. sechellia / D. simulans allele frequency of viable F1 males. We found that recombinant genotypes were rescued when they contained two specific loci from D. simulans - a region containing previously identified Lethal hybrid rescue (Lhr), and an unknown region of chromosome 3L which we name Sechellia aversion to hybrid rescue (Satyr). Our results show that the genetic basis for the recent evolution of this hybrid incompatibility is simple rather than a highly dispersed effect. Further, these data suggest that fixation of differences at Lhr after the split of the D. simulans clade strengthened the hybrid incompatibility between D. sechellia and D. melanogaster.

evolutionary biology↗

Recurrent losses and rapid evolution of the condensin II complex in insects

Condensins play a crucial role in the organization of genetic material by compacting and disentangling chromosomes. The condensin I and condensin II complexes are widely considered to have distinct functions based on studies in a few model organisms, although the specific functions of each complex are yet to be fully understood. The condensin II complex is critical for genome organization in Drosophila, and is a key anti-pairing factor that separates homologous chromosomes in somatic cells. Intriguingly, the Cap-G2 subunit of condensin II is absent in Drosophila melanogaster, and this loss may be related to the high levels of homologous chromosome pairing in somatic cells seen in flies. Here, we find that this Cap-G2 loss predates the origin of Dipterans, and other CapG2 losses have occurred independently in multiple insect lineages. Furthermore, the Cap-H2 and Cap-D3 subunits have also been repeatedly and independently lost in several insect orders, and some taxa lack condensin II-specific subunits entirely. We used Oligopaint DNA-FISH to quantify pairing levels in ten species across seven orders, representing several different configurations of the condensin II complex. We find that all non-Dipteran insects display near-uniform low pairing levels, suggesting that some key aspects of genome organization are robust to condensin II subunit losses. Finally, we observe consistent signatures of positive selection in condensin II subunits across flies and mammals. These findings suggest that these ancient complexes are far more evolutionarily labile than previously suspected, and are at the crossroads of several forms of genomic conflicts. Our results raise fundamental questions about the specific functions of the two condensin complexes and the interplay between them in taxa that have experienced subunit losses, and open the door to further investigations to elucidate the diversity of molecular mechanisms that underlie genome organization across various life forms.

evolutionary biology↗

Altered chromatin localization of hybrid lethality proteins in Drosophila

Understanding hybrid incompatibilities is a fundamental pursuit in evolutionary genetics. In crosses between Drosophila melanogaster females and Drosophila simulans males, the interaction of at least three genes is necessary for hybrid male lethality: Hmr mel, Lhr sim, and gfzf sim. All three hybrid incompatibility genes are chromatin associated factors. While HMR and LHR physically bind each other and function together in a single complex, the connection between either of these proteins and gfzf remains mysterious. Here, we investigate the allele specific chromatin binding patterns of gfzf. First, our cytological analyses show that there is little difference in protein localization of GFZF between the two species except at telomeric sequences. In particular, GFZF binds the telomeric retrotransposon repeat arrays, and the differential binding of GFZF at telomeres reflects the rapid changes in sequence composition at telomeres between D. melanogaster and D. simulans. Second, we investigate the patterns of GFZF and HMR co-localization and find that the two proteins do not normally co-localize in D. melanogaster. However, in inter-species hybrids, HMR shows extensive mis-localization to GFZF sites, and this altered localization requires the presence of gfzf sim. Third, we find by ChIP-Seq that over-expression of HMR and LHR within species is sufficient to cause HMR to mis-localize to GFZF binding sites, indicating that HMR has a natural low affinity for GFZF sites. Together, these studies provide the first insights into the different properties of gfzf between D. melanogaster and D. simulans as well as a molecular interaction between gfzf and Hmr in the form of altered protein localization.

molecular biology↗

Parallel evolution of sperm hyper-activation Ca2+ channels

Sperm hyper-activation is a dramatic change in sperm behavior where mature sperm burst into a final sprint in the race to the egg. The mechanism of sperm hyper-activation in many metazoans, including humans, consists of a jolt of Ca2+ into the sperm flagellum via CatSper ion channels. Surprisingly, CatSper genes have been independently lost in several animal lineages. In Drosophila, sperm hyper-activation is performed through the co-option of the polycystic kidney disease 2 (Dpkd2) Ca2+ channel. The parallels between CatSpers in primates and Dpkd2 in Drosophila provide a unique opportunity to examine the molecular evolution of the sperm hyper-activation machinery in two independent, nonhomologous calcium channels separated by more than 500 million years of divergence. Here, we use a comprehensive phylogenomic approach to investigate the selective pressures on these sperm hyper-activation channels. First, we find that the entire CatSper complex evolves rapidly under recurrent positive selection in primates. Second, we find that pkd2 has parallel patterns of adaptive evolution in Drosophila. Third, we show that this adaptive evolution of pkd2 is driven by its role in sperm hyper-activation. These patterns of selection suggest that the evolution of the sperm hyper-activation machinery is driven by sexual conflict with antagonistic ligands that modulate channel activity. Together, our results add sperm hyper-activation channels to the class of fast evolving reproductive proteins and provide insights into the mechanisms used by the sexes to manipulate sperm behavior.

evolutionary biology↗