Nonindigenous members of the Daphnia pulex complex have been found in many lakes in New Zealand (NZ) in the past 20 years, suggesting a recent invasion. However, very little is known about the precise phylogenetic origin of invasive Daphnia, whether each lake is invaded by a single clone or multiple clones, the lineage of the invasive clones, and whether they are obligately asexual clones. Furthermore, the source and time of arrival of the invasive genotype(s) are unclear. We address these questions by genomic sequencing of Daphnia populations from 13 lakes in the South Island and 1 lake in the North Island, NZ. All biallelic sites in these NZ populations have similar numbers of reads for the two parental alleles, suggesting each NZ population originates from a single asexual clone. Based on 25,643 monomorphic lineage-specific markers, the invasive Daphnia in the South Island were found to be Daphnia pulicaria Forbes, while those in the North Island are hybrids of D. pulicaria Forbes and D. cf. pulex sensu Hebert. Both the South and North Island Daphnia are phylogenetically clustered with North American Daphnia, thereby suggesting their North American origins. We found also that all South Island clones contain identical mitochondrial genomes, suggesting the origin and proliferation from a single founder clone, which we experimentally verified to be an obligate asexual. Estimates from molecular data imply a colonization time for the South Island clones of ~ 60 years ago, with a likely invasion route associated with the introduction of salmonids from North America.
more »
« less
Genome-Wide Allele-Specific Expression in Obligately Asexual Daphnia pulex and the Implications for the Genetic Basis of Asexuality
Abstract Although obligately asexual lineages are thought to experience selective disadvantages associated with reduced efficiency of fixing beneficial mutations and purging deleterious mutations, such lineages are phylogenetically and geographically widespread. However, despite several genome-wide association studies, little is known about the genetic elements underlying the origin of obligate asexuality and how they spread. Because many obligately asexual lineages have hybrid origins, it has been suggested that asexuality is caused by the unbalanced expression of alleles from the hybridizing species. Here, we investigate this idea by identifying genes with allele-specific expression (ASE) in a Daphnia pulex population, in which obligate parthenogens (OP) and cyclical parthenogens (CP) coexist, with the OP clones having been originally derived from hybridization between CP D. pulex and its sister species, Daphnia pulicaria. OP D. pulex have significantly more ASE genes (ASEGs) than do CP D. pulex. Whole-genomic comparison of OP and CP clones revealed ∼15,000 OP-specific markers and 42 consistent ASEGs enriched in marker-defined regions. Ten of the 42 ASEGs have alleles coding for different protein sequences, suggesting functional differences between the products of the two parental alleles. At least three of these ten genes appear to be directly involved in meiosis-related processes, for example, RanBP2 can cause abnormal chromosome segregation in anaphase I, and the presence of Wee1 in immature oocytes leads to failure to enter meiosis II. These results provide a guide for future molecular resolution of the genetic basis of the transition to ameiotic parthenogenesis.
more »
« less
- Award ID(s):
- 1922914
- PAR ID:
- 10382899
- Editor(s):
- Betancourt, Andrea
- Date Published:
- Journal Name:
- Genome Biology and Evolution
- Volume:
- 13
- Issue:
- 11
- ISSN:
- 1759-6653
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Studies of closely related species with known ecological differences provide exceptional opportunities for understanding the genetic mechanisms of evolution. In this study, we compared population-genomics data between Daphnia pulex and Daphnia pulicaria, two reproductively compatible sister species experiencing ecological speciation, the first largely confined to intermittent ponds and the second to permanent lakes in the same geographic region. Daphnia pulicaria has lower genome-wide nucleotide diversity, a smaller effective population size, a higher incidence of private alleles, and a substantially more linkage disequilibrium than D. pulex. Positively selected genes in D. pulicaria are enriched in potentially aging-related categories such as cellular homeostasis, which may explain the extended life span in D. pulicaria. We also found that opsin-related genes, which may mediate photoperiodic responses, are under different selection pressures in these two species. Genes involved in mitochondrial functions, ribosomes, and responses to environmental stimuli are found to be under positive selection in both species. Additionally, we found that the two species have similar average evolutionary rates at the DNA-sequence level, although approximately 160 genes have significantly different rates in the two lineages. Our results provide insights into the physiological traits that differ within this regionally sympatric sister-species pair that occupies unique microhabitats.more » « less
-
ABSTRACT Shared polymorphisms, loci with identical alleles across species, are of unique interest in evolutionary biology as they may represent cases of selection maintaining ancient genetic variation post‐speciation, or contemporary selection promoting convergent evolution. In this study, we investigate the abundance of shared polymorphism between two members of theDaphnia pulexspecies complex. We test whether the presence of shared mutations is consistent with the action of balancing selection or alternative hypotheses such as hybridization, incomplete lineage sorting or convergent evolution. We analyzed over 2,000 genomes from six taxa in theD. pulexspecies group and examined the prevalence and distribution of shared alleles between the focal species pair, North American and EuropeanD. pulex. We show that North American and EuropeanD. pulexdiverged over 10 million years ago, yet retained tens of thousands of shared polymorphisms. We suggest that the number of shared polymorphisms between North American and EuropeanD. pulexcannot be fully explained by hybridization or incomplete lineage sorting alone. We show that most shared polymorphisms could be the product of convergent evolution, that a limited number appear to be old trans‐specific polymorphisms, and that balancing selection is affecting convergent and ancient mutations alike. Finally, we provide evidence that a blue wavelength opsin gene with trans‐specific polymorphisms has functional effects on behavior and fitness in the wild.more » « less
-
Genetic variants of mitochondrial DNA at the individual (heteroplasmy) and population (polymorphism) levels provide insight into their roles in multiple cellular and evolutionary processes. However, owing to the paucity of genome-wide data at the within-individual and population levels, the broad patterns of these two forms of variation remain poorly understood. Here, we analyze 1,804 complete mitochondrial genome sequences from Daphnia pulex, Daphnia pulicaria, and Daphnia obtusa. Extensive heteroplasmy is observed in D. obtusa, where the high level of intraclonal divergence must have resulted from a biparental-inheritance event, and recombination in the mitochondrial genome is apparent, although perhaps not widespread. Global samples of D. pulex reveal remarkably low mitochondrial effective population sizes, <3% of those for the nuclear genome. In addition, levels of population diversity in mitochondrial and nuclear genomes are uncorrelated across populations, suggesting an idiosyncratic evolutionary history of mitochondria in D. pulex. These population-genetic features appear to be a consequence of background selection associated with highly deleterious mutations arising in the strongly linked mitochondrial genome, which is consistent with polymorphism and divergence data suggesting a predominance of strong purifying selection. Nonetheless, the fixation of mildly deleterious mutations in the mitochondrial genome also appears to be driving positive selection on genes encoded in the nuclear genome whose products are deployed in the mitochondrion.more » « less
-
Abstract Asexual reproduction is ancestral in prokaryotes; the switch to sexuality in eukaryotes is one of the major transitions in the history of life. The study of the maintenance of sex in eukaryotes has raised considerable interest for decades and is still one of evolutionary biology’s most prominent question. The observation that many asexual species are of hybrid origin has led some to propose that asexuality in hybrids results from sexual processes being disturbed because of incompatibilities between the two parental species’ genomes. However, in some cases, failure to produce asexual F1s in the lab may indicate that this mechanism is not the only road to asexuality in hybrid species. Here, we present a mathematical model and propose an alternative, adaptive route for the evolution of asexuality from previously sexual hybrids. Under some reproductive alterations, we show that asexuality can evolve to rescue hybrids’ reproduction. Importantly, we highlight that when incompatibilities only affect the fusion of sperm and egg’s genomes, the two traits that characterize asexuality, namely unreduced meiosis and the initiation of embryogenesis without the incorporation of the sperm’s pronucleus, can evolve separately, greatly facilitating the overall evolutionary route. Taken together, our results provide an alternative, potentially complementary explanation for the link between asexuality and hybridization.more » « less
An official website of the United States government

