Showing papers by "Leo W. Beukeboom published in 2013"

Polyploidy in animals: Effects of gene expression on sex determination, evolution and ecology

Abstract: Polyploidy is rarer in animals than in plants. Why? Since Muller's observation in 1925, many hypotheses have been proposed and tested, but none were able to completely explain this intriguing fact. New genomic technologies enable the study of whole genomes to explain the constraints on or consequences of polyploidization, rather than focusing on specific genes or life history characteristics. Here, we review a selection of old and recent literature on polyploidy in animals, with emphasis on the consequences of polyploidization for gene expression patterns and genomic network interactions. We propose a conceptual model to contrast various scenarios for changes in genomic networks, which may serve as a framework to explain the different evolutionary dynamics of polyploidy in animals and plants. We also present new insights of genetic sex determination in animals and our emerging understanding of how animal sex determination systems may hamper or enable polyploidization, including some recent data on haplodiploids. We discuss the role of polyploidy in evolution and ecology, using a gene regulation perspective, and conclude with a synopsis regarding the effects of whole genome duplications on the balance of genomic networks. See also the sister articles focusing on plants by Ashman et al. and Madlung and Wendel in this themed issue.

Adaptive latitudinal cline of photoperiodic diapause induction in the parasitoid Nasonia vitripennis in Europe

Abstract: Living in seasonally changing environments requires adaptation to seasonal cycles. Many insects use the change in day length as a reliable cue for upcoming winter and respond to shortened photoperiod through diapause. In this study, we report the clinal variation in photoperiodic diapause induction in populations of the parasitoid wasp Nasonia vitripennis collected along a latitudinal gradient in Europe. In this species, diapause occurs in the larval stage and is maternally induced. Adult Nasonia females were exposed to different photoperiodic cycles and lifetime production of diapausing offspring was scored. Females switched to the production of diapausing offspring after exposure to a threshold number of photoperiodic cycles. A latitudinal cline was found in the proportion of diapausing offspring, the switch point for diapause induction measured as the maternal age at which the female starts to produce diapausing larvae, and the critical photoperiod for diapause induction. Populations at northern latitudes show an earlier switch point, higher proportions of diapausing individuals and longer critical photoperiods. Since the photoperiodic response was measured under the same laboratory conditions, the observed differences between populations most likely reflect genetic differences in sensitivity to photoperiodic cues, resulting from local adaptation to environmental cycles. The observed variability in diapause response combined with the availability of genomic tools for N. vitripennis represent a good opportunity to further investigate the genetic basis of this adaptive trait.

Cuticular hydrocarbon divergence in the jewel wasp Nasonia: evolutionary shifts in chemical communication channels?

Abstract: The evolution and maintenance of intraspecific communication channels constitute a key feature of chemical signalling and sexual communication. However, how divergent chemical communication channels evolve while maintaining their integrity for both sender and receiver is poorly understood. In this study, we compare male and female cuticular hydrocarbon (CHC) profiles in the jewel wasp genus Nasonia, analyse their chemical divergence and investigate their role as species-specific sexual signalling cues. Males and females of all four Nasonia species showed unique, nonoverlapping CHC profiles unambiguously separating them. Surprisingly, male and female phylogenies based on the chemical distances between their CHC profiles differed dramatically, where only male CHC divergence parallels the molecular phylogeny of Nasonia. In particular, N. giraulti female CHC profiles were the most divergent from all other species and very different from its most closely related sibling species N. oneida. Furthermore, although our behavioural assays indicate that female CHC profiles can generally be perceived as sexual cues attracting males in Nasonia, this function has apparently been lost in the highly divergent female N. giraulti CHC profiles. Curiously, N. giraulti males are still attracted to heterospecific, but not to conspecific female CHC profiles. We suggest that this striking discrepancy has been caused by an extensive evolutionary shift in female N. giraulti CHC profiles, which are no longer used as conspecific recognition cues. Our study constitutes the first report of an apparent abandonment of a sexual recognition cue that the receiver did not adapt to.

A new component of the Nasonia sex determining cascade is maternally silenced and regulates transformer expression.

Abstract: Although sex determination is a universal process in sexually reproducing organisms, sex determination pathways are among the most highly variable genetic systems found in nature. Nevertheless, general principles can be identified among the diversity, like the central role of transformer (tra) in insects. When a functional TRA protein is produced in early embryogenesis, the female sex determining route is activated, while prevention of TRA production leads to male development. In dipterans, male development is achieved by prevention of female-specific splicing of tra mRNA, either mediated by X-chromosome dose or masculinizing factors. In Hymenoptera, which have haplodiploid sex determination, complementary sex determination and maternal imprinting have been identified to regulate timely TRA production. In the parasitoid Nasonia, zygotic transformer (Nvtra) expression and splicing is regulated by a combination of maternal provision of Nvtra mRNA and silencing of Nvtra expression in unfertilized eggs. It is unclear, however, if this silencing is directly on the tra locus or whether it is mediated through maternal silencing of a trans-acting factor. Here we show that in Nasonia, female sex determination is dependent on zygotic activation of Nvtra expression by an as yet unknown factor. This factor, which we propose to term womanizer (wom), is maternally silenced during oogenesis to ensure male development in unfertilized eggs. This finding implicates the upstream recruitment of a novel gene in the Nasonia sex determining cascade and supports the notion that sex determining cascades can rapidly change by adding new components on top of existing regulators.

Data from: Development of a Nasonia vitripennis outbred laboratory population for genetic analysis

Abstract: The parasitoid wasp genus Nasonia has rapidly become a genetic model system for developmental and evolutionary biology. The release of its genome sequence led to the development of high-resolution genomic tools, for both interspecific and intraspecific research, which has resulted in great advances in understanding Nasonia biology. To further advance the utility of Nasonia vitripennis as a genetic model system and to be able to fully exploit the advantages of its fully sequenced and annotated genome, we developed a genetically variable and well-characterized experimental population. In this study, we describe the establishment of the genetically diverse HVRx laboratory population from strains collected from the field in the Netherlands. We established a maintenance method that retains genetic variation over generations of culturing in the laboratory. As a characterization of its genetic composition, we provide data on the standing genetic variation and estimate the effective population size (Ne) by microsatellite analysis. A genome-wide description of polymorphism is provided through pooled resequencing, which yielded 417 331 high-quality SNPs spanning all five Nasonia chromosomes. The HVRx population and its characterization are freely available as a community resource for investigators seeking to elucidate the genetic basis of complex trait variation using the Nasonia model system.

Circadian rhythms differ between sexes and closely related species of Nasonia wasps.

Abstract: Activity rhythms in 24 h light-dark cycles, constant darkness, and constant light conditions were analyzed in four different Nasonia species for each sex separately. Besides similarities, clear differences are evident among and within Nasonia species as well as between sexes. In all species, activity in a light-dark cycle is concentrated in the photophase, typical for diurnal organisms. Contrary to most diurnal insect species so far studied, Nasonia follows Aschoff's rule by displaying long (>24 h) internal rhythms in constant darkness but short (<24 h) in constant light. In constant light, N. vitripennis males display robust circadian activity rhythms, whereas females are usually arrhythmic. In contrast to other Nasonia species, N. longicornis males display anticipatory activity, i.e. activity shortly before light-on in a light-dark cycle. As expected, N. oneida shows activity patterns similar to those of N. giraulti but with important differences in key circadian parameters. Differences in circadian activity patterns and parameters between species may reflect synchronization of specific life-history traits to environmental conditions. Scheduling mating or dispersion to a specific time of the day could be a strategy to avoid interspecific hybridization in Nasonia species that live in sympatry.

Absence of Complementary Sex Determination in the Parasitoid Wasp Genus Asobara (Hymenoptera: Braconidae)

Abstract: An attractive way to improve our understanding of sex determination evolution is to study the underlying mechanisms in closely related species and in a phylogenetic perspective. Hymenopterans are well suited owing to the diverse sex determination mechanisms, including different types of Complementary Sex Determination (CSD) and maternal control sex determination. We investigated different types of CSD in four species within the braconid wasp genus Asobara that exhibit diverse life-history traits. Nine to thirteen generations of inbreeding were monitored for diploid male production, brood size, offspring sex ratio, and pupal mortality as indicators for CSD. In addition, simulation models were developed to compare these observations to predicted patterns for multilocus CSD with up to ten loci. The inbreeding regime did not result in diploid male production, decreased brood sizes, substantially increased offspring sex ratios nor in increased pupal mortality. The simulations further allowed us to reject CSD with up to ten loci, which is a strong refutation of the multilocus CSD model. We discuss how the absence of CSD can be reconciled with the variation in life-history traits among Asobara species, and the ramifications for the phylogenetic distribution of sex determination mechanisms in the Hymenoptera.

Cobreeding in the Burying Beetle, Nicrophorus vespilloides: Tolerance Rather Than Cooperation

Abstract: Under intra- and interspecific competition, cooperative behaviour can provide direct fitness benefits if individuals work together to expel intruders. In the burying beetle Nicrophorus vespilloides, a relatively small species, multiple unrelated pairs can breed together, and individuals are weak competitors in interactions when competing with larger individuals of the same species and with larger species of the same genus. In field and laboratory studies, we found that two pairs together attracted significantly fewer congeneric and non-congeneric competitors compared with single pairs. No other benefits were found. Communal breeding had large negative effects on fitness, as there were fewer offspring per pair and a higher chance of injuries. The higher chance of injuries reflected pairs fighting among themselves and not against competitors. These costs are much greater than the small benefit of fewer intruders. Why should a N. vespilloides breeding pair eventually allow another pair to join? A potential partial explanation is that these are not cooperative pairs in the traditional sense, but rather pairs have a higher tolerance for each other. From the resident’s perspective, joining pairs are not expelled because the chance of injury makes the cost of fighting high. Joining others may have unusually low costs in this species because reproductive opportunities arerare,dependent ona resource that is unpredictable in time and space, and residents should be inclined to tolerating new pairs because of the cost of fighting. Thus, for N. vespilloides, communal breeding appears to be ‘making the best of a bad job’, providing some reproduction ratherthan none.