Daven C. Presgraves

Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila

Speciation—the splitting of one species into two—occurs by the evolution of any of several forms of reproductive isolation between taxa, including the intrinsic sterility and inviability of hybrids. Abundant evidence shows that these hybrid fitness problems are caused by incompatible interactions between loci: new alleles that become established in one species are sometimes functionally incompatible with alleles at interacting loci from another species. However, almost nothing is known about the genes involved in such hybrid incompatibilities or the evolutionary forces that drive their divergence. Here we identify a gene that causes epistatic inviability in hybrids between two fruitfly species, Drosophila melanogaster and D. simulans. Our population genetic analysis reveals that this gene—which encodes a nuclear pore protein—evolved by positive natural selection in both species lineages. These results show that a lethal hybrid incompatibility has evolved as a by-product of adaptive protein evolution.

The molecular evolutionary basis of species formation

All plant and animal species arise by speciation — the evolutionary splitting of one species into two reproductively incompatible species. But until recently our understanding of the molecular genetic details of speciation was slow in coming and largely limited to Drosophila species. Here, I review progress in determining the molecular identities and evolutionary histories of several new speciation genes that cause hybrid dysfunction between species of yeast, flies, mice and plants. The new work suggests that, surprisingly, the first steps in the evolution of hybrid dysfunction are not necessarily adaptive.

PATTERNS OF POSTZYGOTIC ISOLATION IN LEPIDOPTERA

Abstract I present patterns characterizing the evolution of intrinsic postzygotic isolation in Lepidoptera by analyzing data from the literature on genetic distance, strength of hybrid sterility and inviability, biogeography, and natural hybridization. Using genetic distance as a proxy for time, I investigate the time‐course of the evolution of postzygotic isolation and the waiting times to particular hybrid fitness problems. The results show that postzygotic isolation increases gradually as species diverge, but that hybrid sterility evolves faster than hybrid inviability. The overwhelming preponderance of female‐specific hybrid problems in Lepidoptera shows that Haldanea rule (the preferential sterility or inviability of the heterogametic sex) is well obeyed. Together the rates and patterns characterizing the accumulation of postzygotic isolation allow several tests of the composite theory of Haldanes rule. Interestingly, comparing these data with those from Drosophila reveals that Haldanes rule for sterility evolves as fast (if not faster) in Lepidoptera. Finally, I show that a substantial fraction of sympatric species hybridizes in nature and that the majority of these suffer some level of hybrid sterility or inviability.

Sex chromosomes and speciation in Drosophila

Two empirical rules suggest that sex chromosomes play a special role in speciation. The first is Haldanes rule - the preferential sterility and inviability of species hybrids of the heterogametic (XY) sex. The second is the disproportionately large effect of the X chromosome in genetic analyses of hybrid sterility. Whereas the causes of Haldanes rule are well established, the causes of the large X-effect have remained controversial. New genetic analyses in Drosophila confirm that the X is a hotspot for hybrid male sterility factors, providing a proximate explanation for the large X-effect. Several other new findings -- on faster X evolution, X chromosome meiotic drive and the regulation of the X chromosome in the male-germline -- provide plausible evolutionary explanations for the large X-effect.

Speciation by postzygotic isolation: forces, genes and molecules

New species arise as reproductive isolation evolves between diverging populations. Here we review recent work in the genetics of postzygotic reproductive isolation—the sterility and inviability of species hybrids. Over the last few years, research has taken two new directions. First, we have begun to learn a good deal about the population genetic forces driving the evolution of postzygotic isolation. It has, for instance, become increasingly clear that conflict‐driven processes, like sexual selection and meiotic drive, may contribute to the evolution of hybrid sterility. Second, we have begun to learn something about the identity and molecular characteristics of the actual genes causing hybrid problems. Although molecular genetic data are limited, early findings suggest that “speciation genes” correspond to loci having normal functions within species and that these loci sometimes diverge as a consequence of evolution in gene regulation. BioEssays 22:1085–1094, 2000.

Male eye span in stalk-eyed flies indicates genetic quality by meiotic drive suppression

In some species, females choose mates possessing ornaments that predict offspring survival. However, sexual selection by female preference for male genetic quality remains controversial because conventional genetic mechanisms maintain insufficient variation in male quality to account for costly preference and ornament evolution. Here we show that females prefer ornaments that indicate genetic quality generated by transmission conflict between the sex chromosomes. By comparing sex-ratio distributions in stalk-eyed fly (Cyrtodiopsis) progeny we found that female-biased sex ratios occur in species exhibiting eye-stalk sexual dimorphism, and female preferences for long eye span,. Female-biased sex ratios result from meiotic drive, the preferential transmission of a ‘selfish’ X-chromosome. Artificial selection for 22 generations on male eye-stalk length in sexually dimorphic C. dalmanni produced longer eye-stalks and male-biased progeny sex ratios in replicate lines. Because male-biased progeny sex ratios occur when a drive-resistant Y chromosome pairs with a driving X chromosome, long eye span is genetically linked to meiotic drive suppression. Male eye span therefore signals genetic quality by influencing the reproductive value of offspring.

Coevolution of sperm and female reproductive tract morphology in stalk–eyed flies

Sperm and female reproductive tract morphology are among the most rapidly evolving characters known in insects. To investigate whether interspecific variation in these traits results from divergent coevolution we examined testis size, sperm length and female reproductive tract morphology for evidence of correlated evolution using 13 species of diopsid stalk–eyed flies. We found that sperm dimorphism (the simultaneous production of two size classes of sperm by individual males) is ancestral and occurs in four genera while sperm monomorphism evolved once and persists in one genus. The length of ‘long–sperm’ types, though unrelated to male body or testis size, exhibits correlated evolution with two regions of the female reproductive tract, the spermathecae and ventral receptacle, where sperm are typically stored and used for fertilization, respectively. Two lines of evidence indicate that ‘short sperm’, which are probably incapable of fertilization, coevolve with spermathecae. First, loss of sperm dimorphism coincides phylogenetically with reduction or loss of spermathecae. Second, evolutionary change in short–sperm length correlates with change in spermathecal size but not spermathecal duct length or ventral receptacle length. Morphological coevolution between sperm and female reproductive tracts is consistent with a history of female–mediated selection on sperm length.

Evolution of the Drosophila nuclear pore complex results in multiple hybrid incompatibilities.

Speciation often involves the evolution of incompatible gene interactions that cause sterility or lethality in hybrids between populations. These so-called hybrid incompatibilities occur between two or more functionally divergent loci. We show that the nucleoporin 160kDa (Nup160) gene of the fruitfly Drosophila simulans is incompatible with one or more factors on the D. melanogaster X chromosome, causing hybrid lethality. Nup160 encodes a nuclear pore complex protein and shows evidence of adaptive evolution. Furthermore, the protein encoded by Nup160 directly interacts with that of another hybrid lethality gene, Nup96, indicating that at least two lethal hybrid incompatibility genes have evolved as byproducts of divergent coevolution among interacting components of the Drosophila nuclear pore complex.

Telomerase activity coevolves with body mass not lifespan.

In multicellular organisms, telomerase is required to maintain telomere length in the germline but is dispensable in the soma. Mice, for example, express telomerase in somatic and germline tissues, while humans express telomerase almost exclusively in the germline. As a result, when telomeres of human somatic cells reach a critical length the cells enter irreversible growth arrest called replicative senescence. Replicative senescence is believed to be an anticancer mechanism that limits cell proliferation. The difference between mice and humans led to the hypothesis that repression of telomerase in somatic cells has evolved as a tumor‐suppressor adaptation in large, long‐lived organisms. We tested whether regulation of telomerase activity coevolves with lifespan and body mass using comparative analysis of 15 rodent species with highly diverse lifespans and body masses. Here we show that telomerase activity does not coevolve with lifespan but instead coevolves with body mass: larger rodents repress telomerase activity in somatic cells. These results suggest that large body mass presents a greater risk of cancer than long lifespan, and large animals evolve repression of telomerase activity to mitigate that risk.

Genome sequencing reveals complex speciation in the Drosophila simulans clade

The three species of the Drosophila simulans clade--the cosmopolitan species, D. simulans, and the two island endemic species, D. mauritiana and D. sechellia--are important models in speciation genetics, but some details of their phylogenetic and speciation history remain unresolved. The order and timing of speciation are disputed, and the existence, magnitude, and timing of gene flow among the three species remain unclear. Here we report on the analysis of a whole-genome four-species sequence alignment that includes all three D. simulans clade species as well as the D. melanogaster reference sequence. The alignment comprises novel, paired short-read sequence data from a single highly inbred line each from D. simulans, D. mauritiana, and D. sechellia. We are unable to reject a species phylogeny with a basal polytomy; the estimated age of the polytomy is 242,000 yr before the present. However, we also find that up to 4.6% of autosomal and 2.2% of X-linked regions have evolutionary histories consistent with recent gene flow between the mainland species (D. simulans) and the two island endemic species (D. mauritiana and D. sechellia). Our findings thus show that gene flow has occurred throughout the genomes of the D. simulans clade species despite considerable geographic, ecological, and intrinsic reproductive isolation. Last, our analysis of lineage-specific changes confirms that the D. sechellia genome has experienced a significant excess of slightly deleterious changes and a dearth of presumed favorable changes. The relatively reduced efficacy of natural selection in D. sechellia is consistent with its derived, persistently reduced historical effective population size.