The genome sequence of the springtail Allacma fusca (Linnaeus, 1758).

We present a genome assembly from an individual male Allacma fusca (the springtail; Arthropoda; Collembola; Symphypleona; Sminthuridae). The genome sequence is 392.8 megabases in span. Most of the assembly is scaffolded into 6 chromosomal pseudomolecules, including the X 1 and X 2 sex chromosomes. The mitochondrial genome has also been assembled and is 14.94 kilobases in length.

Recent Evolution of a Maternally Acting Sex-Determining Supergene in a Fly with Single-Sex Broods.

Sex determination is a key developmental process, yet it is remarkably variable across the tree of life. The dipteran family Sciaridae exhibits one of the most unusual sex determination systems in which mothers control offspring sex through selective elimination of paternal X chromosomes. Whereas in some members of the family females produce mixed-sex broods, others such as the dark-winged fungus gnat Bradysia coprophila are monogenic, with females producing single-sex broods. Female-producing females were previously found to be heterozygous for a large X-linked paracentric inversion (X'), which is maternally inherited and absent from male-producing females. Here, we assembled and characterized the X' sequence. As close sequence homology between the X and X' made identification of the inversion challenging, we developed a k-mer-based approach to bin genomic reads before assembly. We confirmed that the inversion spans most of the X' chromosome (∼55 Mb) and encodes ∼3,500 genes. Analysis of the divergence between the inversion and the homologous region of the X revealed that it originated very recently (<0.5 Ma). Surprisingly, we found that the X' is more complex than previously thought and is likely to have undergone multiple rearrangements that have produced regions of varying ages, resembling a supergene composed of evolutionary strata. We found functional degradation of ∼7.3% of genes within the region of recombination suppression, but no evidence of accumulation of repetitive elements. Our findings provide an indication that sex-linked inversions are driving turnover of the strange sex determination system in this family of flies.

Are asymmetric inheritance systems an evolutionary trap? Transitions in the mechanism of paternal genome loss in the scale insect family Eriococcidae.

Haplodiploidy and paternal genome elimination (PGE) are examples of asymmetric inheritance, where males transmit only maternally inherited chromosomes to their offspring. Under haplodiploidy, this results from males being haploid, whereas under PGE, males inherit but subsequently exclude paternally inherited chromosomes from sperm. Their evolution involves changes in the mechanisms of meiosis and sex determination and sometimes also dosage compensation. As a result, these systems are thought to be an evolutionary trap, meaning that once asymmetric chromosome transmission evolves, it is difficult to transition back to typical Mendelian transmission. We assess whether there is evidence for this idea in the scale insect family Eriococcidae, a lineage with PGE and the only clade with a suggestion that asymmetric inheritance has transitioned back to Mendelian inheritance. We conduct a cytological survey of 13 eriococcid species, and a cytological, genetic, and gene expression analysis of species in the genus Cystococcus, to investigate whether there is evidence for species in this family evolving Mendelian chromosome transmission. Although we find that all species we examined exhibit PGE, the mechanism is extremely variable within Eriococcidae. Within Cystococcus, in fact, we uncover a previously undiscovered type of PGE in scale insects that acts exclusively in meiosis, where paternally inherited chromosomes in males are present, uncondensed, and expressed in somatic cells but eliminated prior to meiosis. Broadly, we fail to find evidence for a reversion from PGE to Mendelian inheritance in Eriococcidae, supporting the idea that asymmetric inheritance systems such as PGE may be an evolutionary trap.

Genomic evidence of paternal genome elimination in the globular springtail Allacma fusca.

Paternal genome elimination-a type of reproduction in which males inherit but fail to pass on their father's genome-evolved independently in 6-8 arthropod clades. Thousands of species, including several important for agriculture, reproduce via this mode of reproduction. While paternal genome elimination is well established in some of the clades, the evidence in globular springtails (Symphypleona) remains elusive, even though they represent the oldest and most species-rich clade putatively reproducing via paternal genome elimination. We sequenced genomic DNA from whole bodies of Allacma fusca males with high fractions (>27.5%) of sperm to conclusively confirm that all the sperm carry 1 parental haplotype only. Although it is suggestive that the single haplotype present in sperm is maternally inherited, definitive genetic proof of the parent of origin is still needed. The genomic approach we developed allows for the detection of genotypic differences between germline and soma in all species with sufficiently high fraction of germline in their bodies. This opens new opportunities for scans of reproductive modes in small organisms.

Gene-rich X chromosomes implicate intragenomic conflict in the evolution of bizarre genetic systems.

Haplodiploidy and paternal genome elimination (HD/PGE) are common in invertebrates, having evolved at least two dozen times, all from male heterogamety (i.e., systems with X chromosomes). However, why X chromosomes are important for the evolution of HD/PGE remains debated. The Haploid Viability Hypothesis posits that X-linked genes promote the evolution of male haploidy by facilitating purging recessive deleterious mutations. The Intragenomic Conflict Hypothesis holds that conflict between genes drives genetic system turnover; under this model, X-linked genes could promote the evolution of male haploidy due to conflicts with autosomes over sex ratios and genetic transmission. We studied lineages where we can distinguish these hypotheses: species with germline PGE that retain an XX/X0 sex determination system (gPGE+X). Because evolving PGE in these cases involves changes in transmission without increases in male hemizygosity, a high degree of X linkage in these systems is predicted by the Intragenomic Conflict Hypothesis but not the Haploid Viability Hypothesis. To quantify the degree of X linkage, we sequenced and compared 7 gPGE+X species' genomes with 11 related species with typical XX/XY or XX/X0 genetic systems, representing three transitions to gPGE. We find highly increased X linkage in both modern and ancestral genomes of gPGE+X species compared to non-gPGE relatives and recover a significant positive correlation between percent X linkage and the evolution of gPGE. These empirical results substantiate longstanding proposals for a role for intragenomic conflict in the evolution of genetic systems such as HD/PGE.

Gene-rich germline-restricted chromosomes in black-winged fungus gnats evolved through hybridization.

Germline-restricted DNA has evolved in diverse animal taxa and is found in several vertebrate clades, nematodes, and flies. In these lineages, either portions of chromosomes or entire chromosomes are eliminated from somatic cells early in development, restricting portions of the genome to the germline. Little is known about why germline-restricted DNA has evolved, especially in flies, in which 3 diverse families, Chironomidae, Cecidomyiidae, and Sciaridae, carry germline-restricted chromosomes (GRCs). We conducted a genomic analysis of GRCs in the fungus gnat Bradysia (Sciara) coprophila (Diptera: Sciaridae), which has 2 large germline-restricted "L" chromosomes. We sequenced and assembled the genome of B. coprophila and used differences in sequence coverage and k-mer frequency between somatic and germline tissues to identify GRC sequence and compare it to the other chromosomes in the genome. We found that the GRCs in B. coprophila are large, gene rich, and have many genes with divergent homologs on other chromosomes in the genome. We also found that 2 divergent GRCs exist in the population we sequenced. GRC genes are more similar in sequence to genes from another Dipteran family (Cecidomyiidae) than to homologous genes from Sciaridae. This unexpected finding suggests that these chromosomes likely arose in Sciaridae through hybridization with a related lineage. These results provide a foundation from which to answer many questions about the evolution of GRCs in Sciaridae, such as how this hybridization event resulted in GRCs and what features on these chromosomes cause them to be restricted to the germline.

Evolutionary Perspectives on Germline-Restricted Chromosomes in Flies (Diptera).

In some eukaryotes, germline soma differentiation involves elimination of parts of the genome from somatic cells. The portions of the genome restricted to the germline often contain genes that play a role in development and function of the germline. Lineages with germline-restricted DNA are taxonomically diverse, and the size of the germline-restricted genome varies substantially. Unfortunately, few of these lineages have been studied in detail. As a result, we understand little about the general evolutionary forces that drive the origin and maintenance of germline-restricted DNA. One of the taxonomic groups where germline-restricted DNA has been poorly studied are the flies (Diptera). In three Dipteran families, Chironomidae, Cecidomyiidae, and Sciaridae, entire chromosomes are eliminated from somatic cells early in embryonic development. Germline-restricted chromosomes are thought to have evolved independently in the Dipteran families and their size, number, and transmission patterns vary between families. Although there is a wealth of cytological studies on these chromosomes in flies, almost no genomic studies have been undertaken. As a result, very little is known about how and why they evolved and what genes they encode. This review summarizes the literature on germline-restricted chromosomes in Diptera, discusses hypotheses for their origin and function, and compares germline-restricted DNA in Diptera to other eukaryotes. Finally, we discuss why Dipteran lineages represent a promising system for the study of germline-restricted chromosomes and propose future avenues of research on this topic.

Population biology of a selfish sex ratio distorting element in a booklouse (Psocodea: Liposcelis).

Arthropods harbour a variety of selfish genetic elements that manipulate reproduction to be preferentially transmitted to future generations. A major ongoing question is to understand how these elements persist in nature. In this study, we examine the population dynamics of an unusual selfish sex ratio distorter in a recently discovered species of booklouse, Liposcelis sp. (Psocodea: Liposcelididae) to gain a better understanding of some of the factors that may affect the persistence of this element. Females that carry the selfish genetic element only ever produce daughters, although they are obligately sexual. These females also only transmit the maternal half of their genome. We performed a replicated population cage experiment, varying the initial frequency of females that harbour the selfish element, and following female frequencies for 20 months. The selfish genetic element persisted in all cages, often reaching very high (and thus severely female-biased) frequencies. Surprisingly, we also found that females that carry the selfish genetic element had much lower fitness than their nondistorter counterparts, with lower lifetime fecundity, slower development and a shorter egg-laying period. We suggest that differential fitness plays a role in the maintenance of the selfish genetic element in this species. We believe that the genetic system in this species, paternal genome elimination, which allows maternal control of offspring sex ratio, may also be important in the persistence of the selfish genetic element, highlighting the need to consider species with diverse ecologies and genetic systems when investigating the effects of sex ratio manipulators on host populations.

Genetics and Genomics of an Unusual Selfish Sex Ratio Distortion in an Insect.

Diverse selfish genetic elements have evolved the ability to manipulate reproduction to increase their transmission, and this can result in highly distorted sex ratios [1]. Indeed, one of the major explanations for why sex determination systems are so dynamic is because they are shaped by ongoing coevolutionary arms races between sex-ratio-distorting elements and the rest of the genome [2]. Here, we use genetic crosses and genome analysis to describe an unusual sex ratio distortion with striking consequences on genome organization in a booklouse species, Liposcelis sp. (Insecta: Psocodea), in which two types of females coexist. Distorter females never produce sons but must mate with males (the sons of nondistorting females) to reproduce [3]. Although they are diploid and express the genes inherited from their fathers in somatic tissues, distorter females only ever transmit genes inherited from their mothers. As a result, distorter females have unusual chimeric genomes, with distorter-restricted chromosomes diverging from their nondistorting counterparts and exhibiting features of a giant non-recombining sex chromosome. The distorter-restricted genome has also acquired a gene from the bacterium Wolbachia, a well-known insect reproductive manipulator; we found that this gene has independently colonized the genomes of two other insect species with unusual reproductive systems, suggesting possible roles in sex ratio distortion in this remarkable genetic system.

Paternal Genome Elimination in Liposcelis Booklice (Insecta: Psocodea).

How sex is determined in insects is diverse and dynamic, and includes male heterogamety, female heterogamety, and haplodiploidy. In many insect lineages, sex determination is either completely unknown or poorly studied. We studied sex determination in Psocodea-a species-rich order of insects that includes parasitic lice, barklice, and booklice. We focus on a recently discovered species of Liposcelis booklice (Psocodea: Troctomorpha), which are among the closest free-living relatives of parasitic lice. Using genetic, genomic, and immunohistochemical approaches, we show that this group exhibits paternal genome elimination (PGE), an unusual mode of sex determination that involves genomic imprinting. Controlled crosses, following a genetic marker over multiple generations, demonstrated that males only transmit to offspring genes they inherited from their mother. Immunofluorescence microscopy revealed densely packed chromocenters associated with H3K9me3-a conserved marker for heterochromatin-in males, but not in females, suggesting silencing of chromosomes in males. Genome assembly and comparison of read coverage in male and female libraries showed no evidence for differentiated sex chromosomes. We also found that females produce more sons early in life, consistent with facultative sex allocation. It is likely that PGE is widespread in Psocodea, including human lice. This order represents a promising model for studying this enigmatic mode of sex determination.

State dependence, personality, and plants: light-foraging decisions in Mimosa pudica (L.).

Plants make foraging decisions that are dependent on ecological conditions, such as resource availability and distribution. Despite the field of plant behavioral ecology gaining momentum, ecologists still know little about what factors impact plant behavior, especially light-foraging behavior. We made use of the behavioral reaction norm approach to investigate light foraging in a plant species that exhibits rapid movement: Mimosa pudica. We explored how herbivore avoidance behavior in M. pudica (which closes its leaflets temporarily when disturbed) is affected by an individual's energy state and the quality of the current environment and also repeatedly tested the behavior of individuals from two seed sources to determine whether individuals exhibit a "personality" (i.e., behavioral syndrome). We found that when individuals are in a low-energy state, they adopt a riskier light-foraging strategy, opening leaflets faster, and not closing leaflets as often in response to a disturbance. However, when plants are in a high-energy state, they exhibit a plastic light-foraging strategy dependent on environment quality. Although we found no evidence that individuals exhibit behavioral syndromes, we found that individuals from different seed sources consistently behave differently from each other. Our results suggest that plants are capable of making state-dependent decisions and that plant decision making is complex, depending on the interplay between internal and external factors.

Maternal transmission, sex ratio distortion, and mitochondria.

In virtually all multicellular eukaryotes, mitochondria are transmitted exclusively through one parent, usually the mother. In this short review, we discuss some of the major consequences of uniparental transmission of mitochondria, including deleterious effects in males and selection for increased transmission through females. Many of these consequences, particularly sex ratio distortion, have well-studied parallels in other maternally transmitted genetic elements, such as bacterial endosymbionts of arthropods. We also discuss the consequences of linkage between mitochondria and other maternally transmitted genetic elements, including the role of cytonuclear incompatibilities in maintaining polymorphism. Finally, as a case study, we discuss a recently discovered maternally transmitted sex ratio distortion in an insect that is associated with extraordinarily divergent mitochondria.