Previous studies on the stalk-eyed fly, Cyrtodiopsis dalmanni, have shown that males with long eye-stalks win contests and are preferred by females, and artificial selection on male relative eye span alters brood sexratios. Subsequent theory proposes that X-linked meiotic drive can catalyse the evolution of mate preferences when drive is linked to ornament genes. Here we test this prediction by mapping meiotic drive and quantitative trait loci (QTL) for eye span. To map QTL we genotyped 24 microsatellite loci using 1228 F2 flies from two crosses between lines selected for long or short eye span. The crosses differed by presence or absence of a drive X chromosome, X D , in the parental male. Linkage analysis reveals that X D dramatically reduces recombination between X and X D chromosomes. In the X D cross, half of the F2 males carried the drive haplotype, produced partially elongated spermatids and female-biased broods, and had shorter eye span. The largest QTL mapped 1.3 cM from drive on the X chromosome and explained 36% of the variation in male eye span while another QTL mapped to an autosomal region that suppresses drive. These results indicate that selfish genetic elements that distort the sex-ratio can influence the evolution of exaggerated traits.
Sex‐ratio (SR) males produce predominantly female progeny because most Y chromosome sperm are rendered nonfunctional. The resulting transmission advantage of XSR chromosomes should eventually cause population extinction unless segregation distortion is masked by suppressors or balanced by selection. By screening male stalk‐eyed flies, Cyrtodiopsis dalmanni, for brood sex ratio we found unique SR alleles at three X‐linked microsatellite loci and used them to determine if SR persists as a balanced polymorphism. We found that XSR/XST females produced more offspring than other genotypes and that SR males had lower sperm precedence and exhibited lower fertility when mating eight females in 24 h. Adult survival was independent of SR genotype but positively correlated with eye span. We infer that the SR polymorphism is likely maintained by a combination of weak overdominance for female fecundity and frequency dependent selection acting on male fertility. Our discovery of two SR haplotypes in the same population in a 10‐year period further suggests that this SR polymorphism may be evolving rapidly.
Although sex chromosome meiotic drive has been observed in a variety of species for over 50 years, the genes causing drive are only known in a few cases, and none of these cases cause distorted sex-ratios in nature. In stalk-eyed flies (Teleopsis dalmanni), driving X chromosomes are commonly found at frequencies approaching 30% in the wild, but the genetic basis of drive has remained elusive due to reduced recombination between driving and non-driving X chromosomes. Here, we used RNAseq to identify transcripts that are differentially expressed between males carrying either a driving X (XSR) or a standard X chromosome (XST), and found hundreds of these, the majority of which are X-linked. Drive-associated transcripts show increased levels of sequence divergence (dN/dS) compared to a control set, and are predominantly expressed either in testes or in the gonads of both sexes. Finally, we confirmed that XSR and XST are highly divergent by estimating sequence differentiation between the RNAseq pools. We found that X-linked transcripts were often strongly differentiated (whereas most autosomal transcripts were not), supporting the presence of a relatively large region of recombination suppression on XSR presumably caused by one or more inversions. We have identified a group of genes that are good candidates for further study into the causes and consequences of sex-chromosome drive, and demonstrated that meiotic drive has had a profound effect on sequence evolution and gene expression of X-linked genes in this species.
SummaryMicrosatellite primers are often developed in one species and used to assess neutral variability in related species. Such analyses may be confounded by ascertainment bias (i.e. a decline in amplification success and allelic variability with increasing genetic distance from the source of the microsatellites). In addition, other factors, such as the size of the microsatellite, whether it consists of perfect or interrupted tandem repeats, and whether it is autosomal or X-linked, can affect variation. To test the relative importance of these factors on microsatellite variation, we examine patterns of amplification and allelic diversity in 52 microsatellite loci amplified from five individuals in each of six populations of Cyrtodiopsis stalk-eyed flies that range from 2 . 2 % to 11 . 2% mitochondrial DNA sequence divergence from the population used for microsatellite development. We find that amplification success and most measures of allelic diversity declined with genetic distance from the source population, in some cases an order of magnitude faster than in birds or mammals. The median and range of the repeat array length did not decline with genetic distance. In addition, for loci on the X chromosome, we find evidence of lower observed heterozygosity compared with loci on autosomes. The differences in variability between X-linked and autosomal loci are not adequately explained by differences in effective population sizes of the chromosomes. We suggest, instead, that periodic selection events associated with X-chromosome meiotic drive, which is present in many of these populations, reduces X-linked variation.
The evolution of eusociality, especially how selection would favor sterility or subfertility of most individuals within a highly social colony, is an unresolved paradox. Eusociality evolved independently in diverse taxa, including insects (all ants and termites; some bees, wasps, thrips, and beetles), snapping shrimp, and naked mole rats. Termites have received comparatively less focus than the haplodiploid Hymenoptera (ants, bees, and wasps); however, they are the only diploid group with highly complex colonies and an extraordinary diversity of castes. In this study we staged encounters between unrelated colonies of primitive dampwood termites, Zootermopsis nevadensis, mimicking natural meetings that occur under bark. During encounters, kings and/or queens were killed and surviving members merged into one colony. After encounters, members of both unrelated colonies cooperated as a single social unit. We determined the colony of origin of replacement reproductives that emerged after death of kings and/or queens. Here, we document that replacement reproductives developed from workers in either or both original colonies, inherited the merged resources of the colony, and sometimes interbred. Because this species shares many characteristics with ancestral termites, these findings demonstrate how ecological factors could have promoted the evolution of eusociality by accelerating and enhancing direct fitness opportunities of helper offspring, rendering relatedness favoring kin selection less critical.ancestral termites ͉ evolution of eusociality ͉ replacement reproductives ͉ selection ͉ Zootermopsis
Stalk-eyed flies (Diptera: Diopsidae) possess eyes at the ends of elongated peduncles, and exhibit dramatic variation in eye span, relative to body length, among species. In some sexually dimorphic species, evidence indicates that eye span is under both intra- and intersexual selection. Theory predicts that isolated populations should evolve differences in sexually selected traits due to drift. To determine if eye span changes as a function of divergence time, 1370 flies from 10 populations of the sexually dimorphic species, Cyrtodiopsis dalmanni and Cyrtodiopsis whitei, and one population of the sexually monomorphic congener, Cyrtodiopsis quinqueguttata, were collected from Southeast Asia and measured. Genetic differentiation was used to assess divergence time by comparing mitochondrial (cytochrome oxidase II and 16S ribosomal RNA gene fragments) and nuclear (wingless gene fragment) DNA sequences for c. five individuals per population. Phylogenetic analyses indicate that most populations cluster as monophyletic units with up to 9% nucleotide substitutions between populations within a species. Analyses of molecular variance suggest a high degree of genetic structure within and among the populations; > 97% of the genetic variance occurs between populations and species while < 3% is distributed within populations, indicating that most populations have been isolated for thousands of years. Nevertheless, significant change in the allometric slope of male eye span on body length was detected for only one population of either dimorphic species. These results are not consistent with genetic drift. Rather, relative eye span appears to be under net stabilizing selection in most populations of stalk-eyed flies. Given that one population exhibited dramatic evolutionary change, selection, rather than genetic variation, appears to constrain eye span evolution.
Coevolution between male and female traits can result from correlated responses to selection or correlated selection on genetically independent traits. This study examines the possibility that traits involved in precopulatory sexual selection may influence the evolution of traits involved in postcopulatory sexual selection due to the existence of correlated selection or correlated responses to selection. Artificial selection on male eye span in Cyrtodiopsis dalmanni, a sexually dimorphic stalk-eyed fly, is used to test for correlated changes in reproductive traits of male and female flies. Flies from replicate lines that had been under selection for 57 generations were matched for age and genotyped at four X-linked microsatellite loci. Egg number and testis size increased with age, but did not differ among lines. Spermathecal areas and duct lengths differed among replicates, but not among selection treatments. Female relative eye span, size of the ventral receptacle and egg size exhibited significant correlated responses to selection on male relative eye span. The absence of any change in sperm length or testis size between lines indicates that changes in female traits are unlikely due to correlated selection mediated by sperm competition. Significant effects of X-linked microsatellite genotypes indicate instead that the correlated responses to selection were due, in part, to X-linked genes in linkage disequilibrium or that exhibit pleiotropy. The presence of nonadditive allelic effects on genetically correlated female traits combined with additive allelic effects on a male ornament provides a previously unrecognized mechanism by which genetic variation could be maintained despite strong sexual selection.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
hi@scite.ai
10624 S. Eastern Ave., Ste. A-614
Henderson, NV 89052, USA
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.