Edward H. Morrow

The Sexually Antagonistic Genes of Drosophila melanogaster

An association between sex-specific fitness and gene expression in the fruit fly provides an estimate of number, identity and function of sexually antagonistic genes in this species.

Experimental Evidence for the Evolution of Numerous, Tiny Sperm via Sperm Competition

Sperm competition, when sperm from different males compete to fertilize a females ova, is a widespread and fundamental force in the evolution of animal reproduction. The earliest prediction of sperm competition theory was that sperm competition selected for the evolution of numerous, tiny sperm, and that this force maintained anisogamy. Here, we empirically test this prediction directly by using selective breeding to generate controlled and independent variance in sperm size and number traits in the cricket Gryllus bimaculatus. We find that sperm size and number are male specific and vary independently and significantly. We can therefore noninvasively screen individuals and then run sperm competition experiments between males that differ specifically in sperm size and number traits. Paternity success across 77 two-male sperm competitions (each running over 30-day oviposition periods) shows that males producing both relatively small sperm and relatively numerous sperm win competitions for fertilization. Decreased sperm size and increased sperm number both independently predicted sperm precedence. Our findings provide direct experimental support for the theory that sperm competition selects for maximal numbers of miniaturized sperm. However, our study does not explain why G. bimaculatus sperm length persists naturally at approximately 1 mm; we discuss possibilities for this sperm size maintenance.

Experimental Evidence Supports a Sex-Specific Selective Sieve in Mitochondrial Genome Evolution

Polymorphisms in the organelle genome have little effect in female flies but do alter gene expression in males. Mitochondria are maternally transmitted; hence, their genome can only make a direct and adaptive response to selection through females, whereas males represent an evolutionary dead end. In theory, this creates a sex-specific selective sieve, enabling deleterious mutations to accumulate in mitochondrial genomes if they exert male-specific effects. We tested this hypothesis, expressing five mitochondrial variants alongside a standard nuclear genome in Drosophila melanogaster, and found striking sexual asymmetry in patterns of nuclear gene expression. Mitochondrial polymorphism had few effects on nuclear gene expression in females but major effects in males, modifying nearly 10% of transcripts. These were mostly male-biased in expression, with enrichment hotspots in the testes and accessory glands. Our results suggest an evolutionary mechanism that results in mitochondrial genomes harboring male-specific mutation loads.

The evolution of sperm length in moths

Sperm form and function remain poorly understood despite being of fundamental biological importance. An instructive approach has been to examine evolutionary associations across comparable taxa between sperm characters and other, potentially selective reproductive traits. We adopt this approach here in a comparative study examining how sperm lengths are associated with male and female reproductive characters across moths. Primary data have revealed Lepidoptera to be an ideal order for examination: there is profound variation in the dimensions (but not organization) of the reproductive traits between closely related species which all share a monophyletic ancestry, for example, eupyrene sperm length varies from 110 to 12675 μm. Eupyrene (normal fertilizing) and apyrene (anucleate and non–fertile) sperm lengths are positively correlated across taxa and both sperm types show positive associations with mating pattern (as measured by the residual testis size). At fertilization, eupyrene sperm must migrate down the often elongated female spermathecal duct from storage to unite with the ovum. Across taxa, the elongation of this duct is associated with increased eupyrene sperm length, suggesting a positive female influence on sperm size since longer, more powerful sperm may be selected to migrate and/or compete successfully down greater ductal lengths. Apyrene sperm length is not associated with female reproductive tract dimensions. However, we found a positive relationship between the residual testis volume and spermathecal volume, suggesting coevolution between male investment in spermatogenesis and the extent of the female sperm storage capacity. Within males, there is a positive association between the two organs which form the ejaculate–containing spermatophore: the testes and the accessory gland. The ‘trade–up’ in investment to these components is discussed in relation to paternal investment and mating patterns.

Costly traumatic insemination and a female counter-adaptation in bed bugs

Male bed bugs pierce females through the body wall and inseminate directly into the body cavity. It has previously been shown that such traumatic insemination carries costs for females, and sexual conflict regarding the mode of insemination should thus propel male–female coevolution. Since males accumulate sexually antagonistic adaptations, females should evolve counter–adaptations that efficiently abate the costs to females of sexual interactions. Yet, unambiguous experimental evidence for female counter–adaptations is lacking. In bed bugs, the spermalege (a highly modified region of the abdomen where the male usually pierces the female) may represent a female counter-adaptation. We assess the female costs of traumatic insemination by varying the rate of insemination on the one hand, and the rate and mode of piercing trauma to females on the other. Our results show that female mating costs are not extreme––elevated mating rate shortened female lifespan but had no significant effect on lifetime egg production. More importantly, additional abdominal piercing in the spermalege had no effect on females whereas even a very low rate of such piercing outside the spermalege reduced female lifetime egg production by 50%. Thus, females are well counter–adapted to the intrusive mode of insemination exhibited by male bed bugs and the costs of elevated mating are comparable with those in other insects, as predicted by theory. We therefore demonstrate that the spermalege efficiently reduces the direct costs of piercing trauma to females, and hence provide experimental evidence for a female counter–adaptation to a sexually antagonistic male trait.

Assessing sexual conflict in the Drosophila melanogaster laboratory model system

We describe a graphical model of interlocus coevolution used to distinguish between the interlocus sexual conflict that leads to sexually antagonistic coevolution, and the intrinsic conflict over mating rate that is an integral part of traditional models of sexual selection. We next distinguish the ‘laboratory island’ approach from the study of both inbred lines and laboratory populations that are newly derived from nature, discuss why we consider it to be one of the most fitting forms of laboratory analysis to study interlocus sexual conflict, and then describe four experiments using this approach with Drosophila melanogaster. The first experiment evaluates the efficacy of the laboratory model system to study interlocus sexual conflict by comparing remating rates of females when they are, or are not, provided with a spatial refuge from persistent male courtship. The second experiment tests for a lag-load in males that is due to adaptations that have accumulated in females, which diminish male-induced harm while simultaneously interfering with a males ability to compete in the context of sexual selection. The third and fourth experiments test for a lag-load in females owing to direct costs from their interactions with males, and for the capacity for indirect benefits to compensate for these direct costs.

Mitochondrial Replacement, Evolution, and the Clinic

Mitochondrial replacement therapy might bear health risks, especially for males. Mitochondrial diseases [often caused by mutations in mitochondrial DNA (mtDNA)] can manifest in a range of severe symptoms, for which there are currently no cures (1). The diseases are passed from mothers to offspring. Intense research efforts have recently focused on a germline therapeutic strategy to prevent the inheritance of disease-causing mitochondria. However, although there has been increased government interest, especially in the United Kingdom, for using this approach to treat patients, there are reasons to believe that it is premature to move this technology into the clinic at this stage.

Assessing putative interlocus sexual conflict in Drosophila melanogaster using experimental evolution

The theoretical foundation of sexually antagonistic coevolution is that females suffer a net fitness cost through their interactions with males. The empirical prediction is that direct costs to female lifetime fecundity will exceed indirect benefits despite a possible increase in the genetic quality of offspring. Although direct costs of males have been repeatedly shown, to date no study has comprehensively tested whether females are compensated for this direct harm through indirect benefits. Here we use experimental evolution to show that a mutation giving Drosophila melanogaster females nearly complete resistance to the direct costs of male courtship and remating, but which also excluded almost all indirect benefits, is strongly favoured by selection. We estimated the selection coefficient favouring the resistance allele to be +20%. These results demonstrate that any indirect benefits that females accrued were not sufficient to counter-balance the direct costs of males, and reinforce a large body of past studies by verifying interlocus sexual conflict in this model system.

Artificial selection and heritability of sperm length in Gryllus bimaculatus

The adaptive significance of variation in sperm size remains poorly understood but there has been even less attention focused on the genetic mechanisms controlling spermatozoal traits (only three species have been studied). Here we explore heritability and artificial selection of sperm length in the cricket Gryllus bimaculatus. Using a within-family selection design we selected sperm with increasing and decreasing sperm size and bred divergence across five generations. Although we recorded no significant parent–offspring heritability, realized heritability from a within-family analysis was significant at 0.52 ± 0.06 SE (P=0.01) and we successfully achieved significant divergence. However, we only achieved a response when the maternal line was incorporated into selection (from the F1 onwards) and our findings therefore suggest that sperm length in G. bimaculatus is a sex-linked trait that is influenced by genes which are active on the female chromosome. Accordingly, sperm length heritability in G. bimaculatus can only be measured using a within-family design because the spermatozoal phenotype is sex-limited (to males) while the genotype is sex-linked (to females). The evolutionary significance of the heritability of sperm length is discussed with reference to sex-linkage of this important sex-limited trait.

Two sexes, one genome: the evolutionary dynamics of intralocus sexual conflict

As the evolutionary interests of males and females are frequently divergent, a trait value that is optimal for the fitness of one sex is often not optimal for the other. A shared genome also means that the same genes may underlie the same trait in both sexes. This can give rise to a form of sexual antagonism, known as intralocus sexual conflict (IASC). Here, a tug-of-war over allelic expression can occur, preventing the sexes from reaching optimal trait values, thereby causing sex-specific reductions in fitness. For some traits, it appears that IASC can be resolved via sex-specific regulation of genes that subsequently permits sexual dimorphism; however, it seems that whole-genome resolution may be impossible, due to the genetic architecture of certain traits, and possibly due to the changing dynamics of selection. In this review, we explore the evolutionary mechanisms of, and barriers to, IASC resolution. We also address the broader consequences of this evolutionary feud, the possible interactions between intra- and interlocus sexual conflict (IRSC: a form of sexual antagonism involving different loci in each sex), and draw attention to issues that arise from using proxies as measurements of conflict. In particular, it is clear that the sex-specific fitness consequences of sexual dimorphism require characterization before making assumptions concerning how this relates to IASC. Although empirical data have shown consistent evidence of the fitness effects of IASC, it is essential that we identify the alleles mediating these effects in order to show IASC in its true sense, which is a “conflict over shared genes.”