bioRxiv Science⌕ Search

Biology subjects

Baird, R. B.

Publications and source records attributed to Baird, R. B..

8 recordsLinked to original sources

Reproductive morph specialisation facilitated by a maternal sex-determining region in a fungus gnat (Bradysia coprophila)

Sexual reproduction is a ubiquitous process in eukaryotes, yet mechanisms of sex determination are strikingly diverse. One unique and understudied system is maternal genetic sex determination (mat-GSD), in which the genotype of the mother determines offspring sex. In some species, mothers further specialise into genetically determined reproductive morphs: gynogenic females that produce all-female broods, and androgenic females that produce all-male broods. Although this partition echoes the evolution of separate, dimorphic sexes, it remains unclear whether the morphs diverge in traits beyond offspring sex determination, and how this affects the evolutionary dynamics of the mating system. Here we address these questions in the dark-winged fungus gnat Bradysia coprophila, in which female morphs are determined by a large X-linked inversion. We show that maternal reproductive morphs diverge significantly in life history traits and gene expression profile, suggesting adaptive specialisation into their reproductive roles. We further evaluate potential drivers for specialisation and test two of them empirically, showing evidence in line with sex-specific maternal provisioning. By drawing explicit parallels with sex chromosome evolution and sexual dimorphism, our results extend core principles of reproductive specialisation to mat-GSD systems, and underscore the potential of unusual reproductive systems for extending fundamental evolutionary theory on how selection and genomic architecture interact to shape mating system evolution.

evolutionary biology↗

Parent-offspring conflict over sex determination in non-Mendelian systems

Across the tree of life, many organisms exhibit asymmetric inheritance systems in which males and females contribute differently to the long-term genetic future of the population. Although, in such groups, the sexes ultimately differ in their contributions, the zygotes that become males and females often start out genetically identical, with sex determined by maternal factors deposited into the embryo. However, there has been little work considering what the optimal sex ratio is from the perspective of the offspring in such scenarios, how this may differ from their parents, and how such conflicts may be modulated by other ecological factors. To investigate this, we develop analytical models to calculate the optimal sex allocation under a range of asymmetric genetic systems, and under the control of different parties. We then investigate the effects of various population structures and mating systems to consider their effects in shaping such conflicts. We find that asymmetric genetic systems may be prone to perpetual ongoing conflict between mothers and offspring over sex determination, even in panmictic populations. This may be one factor explaining the diverse and unusual sets of sex determining systems seen in these groups.

evolutionary biology↗

Distinct satellite DNA composition between core and germline restricted chromosomes in Bradysia (Sciara) coprophila

Programmed DNA elimination (PDE), a phenomenon wherein cells eliminate a subset of genetic material during certain stages of development, is observed in a broad range of organisms. The fungus gnat Bradysia (formerly Sciara) coprophila undergoes a series of PDE events during their development, including elimination of germline-restricted chromosomes (called L chromosomes) in soma and elimination of paternal chromosomes during male meiosis. However, the underlying mechanisms of this phenomenon are poorly understood. Highly repetitive satellite DNA, which often shows chromosome specific distribution, is a possible candidate for sequences involved in PDE. In this study, we utilized recent genomic data and genome assemblies to identify new satellite DNA sequences of B. coprophila. Through characterization of satellite DNA distribution on chromosomes, we found that the X and autosomes do not share centromeric satellite DNA sequence with the L chromosomes. We further provide the cytological evidence that confirms a recent finding based on the genome assembly that there are two distinct L chromosomes that were not previously distinguished cytologically. Together, our work lays a foundation for future studies to explore the possible connection between satellite DNA and the mechanism of PDE in B. coprophila.

cell biology↗

Does non-Mendelian chromosome transmission and unusual sex determination affect male mate choice in the fly Bradysia coprophila?

Mate quality and the cost of mating affect the evolution of mating preferences and is one reason females often show stronger mate preferences than males. Fungus gnats in the family Sciaridae (Diptera) are a family in which we might expect to see the evolution of strong male mate preferences. Many Sciaridae species are monogenic, where females exclusively produce offspring of one sex. Sciaridae species also exhibit paternal genome elimination, a reproductive system where males only transmit maternally inherited chromosomes to offspring. Therefore, Sciaridae males would benefit from exhibiting mating preferences for females that produce female offspring, as a males genes are only transmitted to future generations through his daughters, not his sons. We explore male mate choice in the sciarid fly Bradysia (formerly Sciara) coprophila. We find that mating is costly, as males become sperm limited through multiple matings, and that males exhibit preferences for larger females, suggesting that males are selected to be choosy. However, we do not find male preferences for females that produce female offspring, instead we find that males prefer mating with females that produce male offspring. We speculate that this seemingly maladaptive behaviour may be due to female receptivity rather than male preference, or that males are unable to distinguish between females of different types, which is perhaps surprising since these females differ genetically by 1000s of genes (through a large paracentric inversion on the X chromosome). Together we show how the interplay between unusual genetics and sex determining systems may affect mating system evolution. Summary statementIn the fungus gnat Bradysia coprophila females are genetically predetermined to produce broods of just one sex and males only transmit maternally inherited genes to offspring. These factors suggest males should have strong mating preferences for females that produce daughters, which we explore. We find that while males would benefit from being "choosy", they appear unable to distinguish the two female types, possibly because females are selected to hide their sex determining phenotype.

evolutionary biology↗

Maternal inheritance of primary sex ratios in the dark-winged fungus gnat Lycoriella ingenua

Sex determination mechanisms in insects are extraordinarily diverse, although most species have zygotic genotypic sex determination where sex is established by sex chromosomes upon fertilisation. Dark-winged fungus gnats (Diptera: Sciaridae) are a large and speciose family of flies where sex determination is a result of an unusual interplay of zygotic, maternal, and environmental factors. This causes some species to produce clutches of offspring that deviate considerably from the standard 1:1 Fisherian sex ratio. An early study suggested that these primary sex ratios may be heritable from mother to daughter, but this observation has not been corroborated and the genetic basis for this trait remains unknown. Other studies have found that in some species, there is an additional temperature effect on the primary sex ratio, but again the mechanism is unknown. Here, we perform sibling crosses and temperature-shift experiments in a recently isolated line of the species Lycoriella ingenua and find evidence for highly variable and heritable primary sex ratios, but no significant environmental effect. We discuss the consequences of our findings for understanding the mechanisms that produce these unusual sex ratios, and the evolution of sex determination more broadly in this clade.

evolutionary biology↗

Paternal genome elimination, monogenic reproduction, and the evolutionary genetics of atypical sex chromosome systems

Sex chromosomes differ from autosomes in both their ploidy and transmission genetics. Consequently, selection, mutation, and drift may act differently upon them, driving distinct patterns in genetic divergence, diversity, and gene content. Recently, researchers have begun to consider a wider set of organisms with non-standard inheritance and sex-determination systems, however in many cases we lack theory which extends to such cases. One such example is paternal genome elimination (PGE), an unusual reproductive system which has independently evolved in two fly families, the fungus gnats (Sciaridae) and gall midges (Cecidomyiidae), and one order of springtails (Symphypleona). Under PGE, males receive but do not transmit a paternal genome, such that the autosomes and X chromosomes exhibit the same transmission genetics, but with different somatic ploidy. This makes them uniquely suited to test hypotheses about the role of haploid selection in males. Additionally, repeatedly throughout these groups a novel sex determination system - monogeny - has evolved, whereby females produce broods of exclusively one sex. The genetic basis of monogeny partitions the X chromosome into three segments, all displaying distinct inheritance patterns. Here we develop a series of theoretical models adapted to the genetics of these groups, generating testable predictions as to the relative genetic diversity within populations, and divergence between populations. Our results suggest that these species are excellent systems with which to test many fundamental principles in evolutionary genetics.

evolutionary biology↗

Genetic drift drives faster-Z evolution in the salmon louse Lepeophtheirus salmonis

Sex chromosome evolution is a particularly complex sub-field of population genetics and there are still unresolved questions about how quickly and adaptively these chromosomes should evolve compared to autosomes. One key limitation to existing knowledge is an intense focus on only a handful of taxa in existing literature, resulting in uncertainty about whether observed patterns reflect general processes or are idiosyncratic to the more widely studied clades. In particular, the Z chromosomes of female heterogametic (ZW) systems tend to be quickly but not adaptively evolving in birds, while in butterflies and moths Z chromosomes tend to be evolving adaptively, but not always faster than autosomes. To understand how these two observations fit into broader evolutionary patterns, we explore, for the first time, patterns of Z chromosome evolution outside of these two well-studied clades. We utilize a publicly available high quality genome, gene expression, population, and outgroup data for the salmon louse Lepeophtheirus salmonis, an important aquacultural pest copepod. We find that the Z chromosome is faster evolving than the autosomes, but that this increased effect is driven by drift rather than adaptive evolution. This faster-Z effect seems to be a result of a very low effective population size of the Z chromosome, as well as high rates of female reproductive failure contributing to decreased efficiency of hemizygous selection acting on the Z. These results highlight the usefulness of organismal life history in calibrating population genetic expectations and demonstrate the usefulness of the ever-expanding wealth of modern publicly available genomic data to help resolve outstanding evolutionary questions.

evolutionary biology↗

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 (approximately 55Mb) and encodes around 3500 genes. Analysis of the divergence between the inversion and the homologous region of the X revealed that it originated very recently (<0.5 mya). 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 around 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.

evolutionary biology↗