Biology subjects

Beukeboom, L.

Publications and source records attributed to Beukeboom, L..

6 recordsLinked to original sources

bioRxiv2026

X-Y divergence of house fly (Musca domestica) proto-sex chromosomes follows distinct evolutionary trajectories despite residing in the same genome

Sex determination systems and sex chromosomes frequently differ between species. One cause of these differences is new sex determining genes that drive evolutionary turnover of sex chromosomes. At the earliest stages of this turnover, X and Y (or Z and W) chromosomes start out as nearly identical homologs, and they can diverge via chromosomal rearrangements (e.g., inversions) that suppress X-Y recombination. However, multiple examples from across animals and plants provide exceptions to this canonical model of sex chromosome evolution. For example, some X-Y pairs remain undifferentiated for long evolutionary time periods, while other sex chromosomes become differentiated without chromosomal rearrangements. How or why these non-canonical trajectories occur remains elusive, despite increasing evidence of their pervasiveness. The house fly, Musca domestica, is a well-suited system to address this gap because all six chromosomes can be a Y, providing multiple replicates of a natural experiment within a single genomic environment. To test for canonical and non-canonical evolutionary trajectories, we generated haplotype-resolved chromosome-level assemblies from five strains of the house fly, each of which carries a different Y chromosome (IM, IIM, IIIM, VM, and YM). We identified an inversion on only one of the sex chromosomes (IIM), which was associated with elevated X-Y divergence but did not capture the male-determining locus. In contrast, there was X-Y divergence across almost the entire length of the IM, IIIM, and VM sex chromosomes, despite no detectable inversions. YM was the only sex chromosome to contain substantial Y-specific sequences, which were limited to a segment on one end of the chromosome containing the male-determining gene. This YM chromosome, and its corresponding X, were highly diverged from the X chromosome found in many other flies (Muller element F), despite a strong cytological resemblance. This study highlights how multiple different canonical and non-canonical modes of sex chromosome evolution can co-exist within a single genome.

genomics↗

bioRxiv2020

Temperature-dependent effects of house fly proto-Y chromosomes on gene expression act independently of the sex determination pathway

Sex determination, the developmental process by which sexually dimorphic phenotypes are established, evolves fast. Species with polygenic sex determination, in which master regulatory genes are found on multiple different proto-sex chromosomes, are informative models to study the evolution of sex determination. House flies are such a model system, with male determining loci possible on all six chromosomes and a female-determiner on one of the chromosomes as well. The two most common male-determining proto-Y chromosomes form latitudinal clines on multiple continents, suggesting that temperature variation is an important selection pressure responsible for maintaining polygenic sex determination in this species. To identify candidate genes that may be under selection, we used RNA-seq to test for temperature-dependent effects of the proto-Y chromosomes on gene expression in adult house flies. We find no evidence for ecologically meaningful temperature-dependent expression of sex determining genes between male genotypes, but we were likely not sampling an appropriate developmental time-point to identify such effect. In contrast, we identified many other genes whose expression depends on the interaction between proto-Y chromosome genotype and temperature, including genes that encode proteins involved in reproduction, metabolism, lifespan, stress response, and immunity. Notably, genes with genotype-by-temperature interactions on expression are not enriched on the proto-sex chromosomes. Moreover, there is no evidence that temperature-dependent expression is driven by chromosome-wide expression divergence between the proto-Y and proto-X alleles. Therefore, if temperature-dependent gene expression is responsible for differences in phenotypes and fitness of proto-Y genotypes across house fly populations, these effects are driven by a small number of temperature-dependent alleles on the proto-Y chromosomes that may in turn affect the expression of genes on other chromosomes.

evolutionary biology↗

bioRxiv2019

Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum

BackgroundParasitoid wasps have fascinating life cycles and play an important role in trophic networks, yet little is known about their genome content and function. Parasitoids that infect aphids are an important group with the potential for biocontrol, and infecting aphids requires overcoming both aphid defenses and their defensive endosymbionts. ResultsWe present the de novo genome assemblies, detailed annotation, and comparative analysis of two closely related parasitoid wasps that target pest aphids: Aphidius ervi and Lysiphlebus fabarum (Hymenoptera: Braconidae: Aphidiinae). The genomes are small (139 and 141 Mbp), highly syntenic, and the most AT-rich reported thus far for any arthropod (GC content: 25.8% and 23.8%). This nucleotide bias is accompanied by skewed codon usage, and is stronger in genes with adult-biased expression. AT-richness may be the consequence of reduced genome size, a near absence of DNA methylation, and age-specific energy demands. We identify expansions of F-box/Leucine-rich-repeat proteins, suggesting that diversification in this gene family may be associated with their broad host range or with countering defenses from aphids endosymbionts. The absence of some immune genes (Toll and Imd pathways) resembles similar losses in their aphid hosts, highlighting the potential impact of symbiosis on both aphids and their parasitoids. ConclusionsThese findings are of fundamental interest for insect evolution and beyond. This will provide a strong foundation for further functional studies including coevolution with respect to their hosts, the basis of successful infection, and biocontrol. Both genomes are available at https://bipaa.genouest.org.

genomics↗

bioRxiv2019

Genetic architecture of male courtship behavior differences in the parasitoid wasp genus Nasonia (Hymenoptera; Pteromalidae)

Very little is known about the genetic basis of behavioral variation in courtship behavior, which can contribute to speciation by prezygotic isolation of closely related species. Here, we analyze the genetic basis and architecture of species differences in the male courtship behavior of two closely related parasitoid wasps Nasonia vitripennis and N. longicornis. Both species occur microsympatrically in parts of their ranges and have been found in the same host pupae. Despite strong postzygotic isolation mechanisms between these two Nasonia species, viable hybrid females can be produced in the laboratory if both species are cured of their Wolbachia endosymbionts. We used haploid F2 hybrid males derived from virgin F1 hybrid females of two independent mapping populations to study the genetic architecture of five quantitative and two qualitative components of their courtship behavior. A total of 14 independent Quantitative Trait Loci (QTL) were found in the first mapping population (320 males), which explained 4-25% of the observed phenotypic variance. Ten of these QTL were confirmed by a second independent mapping population (112 males) and no additional ones were found. A genome-wide scan for two-loci interactions revealed many unique but mostly additive interactions explaining an additional proportion of the observed phenotypic variance. Courtship QTL were found on all five chromosomes and four loci were associated with more than one QTL, indicating either possible pleiotropic effects of individual QTL or individual loci contributing to multiple courtship components. Our results indicate that these two evolutionary young species have rapidly evolved multiple significant phenotypic differences in their courtship behavior that have a polygenic and highly interactive genetic architecture. Based on the location of the QTL and the published Nasonia genome sequence we were able to identify a series of candidate genes for further study.

genetics↗

bioRxiv2019

Latitudinal variation in circadian rhythmicity in Nasonia vitripennis

Many physiological processes of living organisms show circadian rhythms, governed by an endogenous clock. This clock has a genetic basis and is entrained by external cues such as light and temperature. Other physiological processes exhibit seasonal rhythms, that are also responsive to light and temperature. We previously reported a natural latitudinal cline of photoperiodic diapause induction in the parasitic wasp Nasonia vitripennis in Europe and a correlated haplotype frequency for the circadian clock gene period (per). To evaluate if this correlation is reflected in circadian behaviour, we investigated circadian locomotor activity of seven populations from the cline. We found that the proportion of rhythmic males is higher than females in constant darkness, and that mating decreased rhythmicity of both sexes. Only for virgin females, the free running period ({tau}) increased weakly with latitude. Wasps from the most southern locality had an overall shorter free running rhythm and earlier onset, peak and offset of activity during the 24 h period, than wasps from the northernmost locality. We evaluate this variation in rhythmicity as a function of period haplotype frequencies in the populations and discuss its functional significance in the context of local adaptation.

evolutionary biology↗

bioRxiv2019

Minimal effects of proto-Y chromosomes on house fly gene expression in spite of evidence that selection maintains stable polygenic sex determination

Sex determination is the developmental process by which organismal sex is established. Sex determination evolves fast, often due to changes in the master regulators at the top of the pathway. In addition, some species are polymorphic for multiple different master regulators within natural populations. Understanding the forces that maintain this polygenic sex determination can be informative of the factors that drive the evolution of sex determination. The house fly, Musca domestica, is a well-suited model to those ends because natural populations harbor male-determining loci on each of the six chromosomes and a bi-allelic female-determiner. Multiple lines of evidence suggest that natural selection maintains polygenic sex determination in house fly. However, previous work found that there are very few sequence differences between proto-Y chromosomes and their homologous X chromosomes. This suggests that there is not much genetic variation upon which natural selection could act to maintain polygenic sex determination in house fly. To address this paradox, we performed RNA-seq experiments that examine the effects of the two most common proto-Y chromosomes on gene expression. We find that the proto-Y chromosomes do indeed have a relatively minor effect on gene expression, as expected based on the minimal X-Y sequence differences. Despite these minimal gene expression differences, we identify some patterns that are consistent with sex-specific selection acting on phenotypic effects of proto-Y chromosomes. Our results suggest that, if natural selection maintains polygenic sex determination in house fly, the phenotypic differences under selection are minor and possibly depend on ecological contexts that were not tested in our experimental design.

genomics↗