Inter-island divergence within Drosophila mauritiana, a species of the D. simulans complex: Past history and/or speciation in progress?

Speciation with gene flow may be more common than generally thought, which makes detailed understanding of the extent and pattern of genetic divergence between geographically isolated populations useful. Species of the Drosophila simulans complex provide a good model for speciation and evolutionary studies, and hence understanding their population genetic structure will increase our understanding of the context in which speciation has occurred. Here, we describe genetic diversity and genetic differentiation of two distant populations of D. mauritiana (Mauritius and Rodrigues Islands) at mitochondrial and nuclear loci. We surveyed the two populations for their mitochondrial haplotypes, eight nuclear genes and 18 microsatellite loci. A new mitochondrial type is fixed in the Rodrigues population of D. mauritiana. The two populations are highly differentiated, their divergence appears relatively ancient (100,000 years) compared to the origin of the species, around 0.25MYA, and they exhibit very limited gene flow. However, they have similar levels of divergence from their sibling, D. simulans. Both nuclear genes and microsatellites revealed contrasting demographic histories between the two populations, expansion for the Mauritius population and stable population size for the Rodrigues Island population. The discovery of pronounced geographic structure within D. mauritiana combined to genetic structuring and low gene flow between the two island populations illuminates the evolutionary history of the species and clearly merits further attention in the broad context of speciation.

Pollen and sperm heteromorphism: convergence across kingdoms?

Sperm competition theory predicts that males should produce many, similar sperm. However, in some species of animals and plants, males exhibit a heteromorphism that results in the production of at least two different types of sperm or pollen grains. In animals, sperm heteromorphism typically corresponds to the production of one fertile morph and one (or more) sterile morph(s), whereas in plants two or more pollen morphs (one of which can be either sterile or fertile) are produced in all flowers but sometimes in different anthers. Heteromorphism has arisen independently several times across phyla and at different phylogenetic levels. Here, we compare and contrast sperm and pollen heteromorphism and discuss the evolutionary hypotheses suggested to explain heteromorphism in these taxa. These hypotheses include facilitation, nutritive contribution, blocking, cheap filler, sperm flushing or killing for animals; outcrossing and precise cross-pollen transfer or bet-hedging strategy for plants; cryptic female choice for both. We conclude that heteromorphism in the two phyla is most likely linked to a general evolutionary response to sexual selection, either to increase one male's sperm or pollen success in competition with other males, or mediate male/female interactions. Therefore, although sperm and pollen are not homologous, we suggest that heteromorphism represents an example of convergence across kingdoms.

Divergence between Drosophila santomea and allopatric or sympatric populations of D. yakuba using paralogous amylase genes and migration scenarios along the Cameroon volcanic line.

We have used two paralogous genes (Amyrel and Amy) of the amylase multigene family to reconstruct the phylogeny of the nine Drosophila melanogaster subgroup sister species, including D. santomea, the newly discovered endemic from São Tomé island. The evolutionary divergence of these genes is of special interest as it is suspected to result from physiological evolution via gene duplication. This paper describes the relationship between the geographical origin of the various strains and the patterns of mating and phylogeny, focusing on the evolution of D. santomea and its relationship to other species and their niches. The Amyrel and Amy data indicate that, contrary to expectations, the sympatric insular D. yakuba population is less closely related to D. santomea than allopatric mainland ones, suggesting that the extant insular D. yakuba population on São Tomé results from a recent secondary colonization. Data for sympatric and allopatric D. yakuba suggest that D. santomea arose from a mainland D. yakuba parental stock when montane habitats of the Cameroon volcanic line extended to lower altitudes during colder and less humid periods. Despite their different modes of evolution and different functions, the Amyrel and Amy genes provide remarkably consistent topologies and hence reflect the same history, that of the species.

Fragmented forests, evolving flies: molecular variation in African populations of Drosophila teissieri.

Microsatellite variation from eight loci was studied in five populations of Drosophila teissieri, a fruit-fly found only in the rain forests of sub-Saharan Africa. Five noncontiguous rain forest sites (from Tanzania, Gabon and Ivory Coast) were sampled to measure the effects of historical forest fragmentation on population structure in an obligatory forest-dwelling species. The Ivory Coast and Gabon populations showed a wider range of alleles, different modal alleles and had a higher genetic diversity than the three East African populations. As could be expected, genetic differentiation (FST) was significantly correlated with physical distance, but the westernmost population (Ivory Coast) showed values that were intermediate between the central (Gabon) and Eastern (Tanzania) populations. A migration-drift equilibrium in a stable continuum of populations did not appear adequate to describe the observed distribution. It seems probable that the species has undergone abrupt changes involving isolation, merging and migration of populations, as a consequence of repeated waves of forest fragmentation and coalescence.

Evolutionary novelties in islands: Drosophila santomea, a new melanogaster sister species from São Tomé.

The finding of new melanogaster sister species may help us in understanding more about how the emergence of genetic novelties, particularly in insular habitats, can result in speciation. Here we report on the discovery of Drosophila santomea, which is the first melanogaster sibling found off West-equatorial Africa, on São Tomé, one of the Gulf of Guinea islands. Although the eight other melanogaster sister species are remarkably conservative in their morphology except for their terminalia, the new find has a morphological trait distinguishing it from all of these: a pure yellow body coloration of both sexes without the normal black abdominal banding. Evidence from the terminalia, polytene and mitotic chromosomes, period gene and allozymes are provided indicating that it is nonetheless the nearest relative of Drosophila yakuba with which it coexists on the island. The new find is a clear-cut taxon as shown by the production of sterile male hybrids, eventually with developmental defects, in both directions of cross with yakuba and by the existence of an altitudinal divide accompanied by a hybrid zone at mid-elevation on the island. Molecular and karyotypic data further support this conclusion. In contrast to the significant divergence of their nuclear DNAs, an intriguing similarity in their cytochrome b sequences was observed indicating a recent coalescence common to santomea, yakuba and also teissieri cytoplasms. These were shown to harbour the same Wolbachia endosymbiotic bacteria which could possibly be responsible for mitochondrial DNA hitchhiking across the species barrier.

Molecular evidence for parallel evolution of adaptive syndromes in fig-breeding Lissocephala (Drosophilidae).

Afrotropical Lissocephala (Drosophilidae) breed strictly in syconia (figs) of Ficus (Moraceae) and have accordingly evolved specific features including modified female and eggshell morphologies, ovipositing, larval foraging, and mating behaviors. These various traits may exist as two or three alternative states. Each species displays a specific suite of traits so closely coordinated with one another that alternative states of the overall suites of traits can be seen as "adaptive syndromes." Three clear-cut adaptive syndromes can be recognized while two taxonomic lineages (juncta and sanu species groups) are traditionally accepted on the basis of male terminalia. A crucial evolutionary question results from the consideration that ecological clusters and taxonomic groups have conflicting compositions: the three syndromes are found in the juncta group while two of them occur in the sanu group. To resolve this conflict, we present molecular data which provide a robust phylogeny: mitochondrial DNA (12S + 16S ribosomal DNA and cytochrome b) sequence data are in agreement with one another regardless of the algorithm used. All molecular data consistently support male terminalia dichotomy. Such a level of consistency unambiguously indicates that parallel evolution of adaptive syndromes occurred. Thus, homoplasy may affect morphological and behavioral traits concomitantly when these are involved in a network of functional relationships.

Another way of being anisogamous in Drosophila subgenus species: giant sperm, one-to-one gamete ratio, and high zygote provisioning.

It is generally assumed that sexes in animals have arisen from a productivity versus provisioning conflict; males are those individuals producing gametes necessarily small, in excess, and individually bereft of all paternity assurance. A 1- to 2-cm sperm, 5-10 times as long as the male body, might therefore appear an evolutionary paradox. As a matter of fact, species of Drosophila of the Drosophila subgenus differ from those of other subgenera by producing exclusively sperm of that sort. We report counts of such giant costly sperm in Drosophila littoralis and Drosophila hydei females, indicating that they are offered in exceedingly small amounts, tending to a one-to-one gamete ratio after a single mating. As a result, most of them are successfully involved in a fertilization. Hence, the concept of "paternity assurance of individual sperm" arises. Evidence is further provided here that almost the entire sperm is incorporated into the egg during fertilization. Labeling with specific antibodies in fertilized eggs reveals intact axonemes up to late gastrulation. The question, then, is why selection has favored such an unusual strategy. Explanations related to some prefertilization functions are ruled out. It is therefore tentatively proposed that virtually every giant sperm constitutes a "direct paternal legacy to the embryo," which, in contrast to any male-derived nuptial gift, cannot be minimized by female remating. We suggest that dramatic shortage of giant sperm with a high prospect of fusion and increased zygote provisioning is merely another way of being anisogamous.

Can we predict the mating pattern of Drosophila females from the sperm length distribution in males?

In order to test the validity of the prediction of the mating pattern of females from the sperm length distribution in males, three species of Drosophila were analysed. Males in the three species are equally polygynous but females differ in the level of polyandry. A 'low recurrence polyandry' is observed in the sperm dimorphic species D. affinis while a 'high recurrence polyandry' is observed in the sperm monomorphic species D. latifasciaeformis and D. littoralis. These results are consistent with the hypothesis proposed previously that sperm dimorphism in males can only be maintained by a selective alternative in females (i.e. facultative female polygamy), whereas a stricter mating system (e.g. 'obligatory' polyandry) should only result in sperm monomorphism irrespective of the absolute value of sperm length.

Comparative kinetics of short and long sperm in sperm dimorphic Drosophila species.

All species of the Drosophila obscura group exhibit within-ejaculate sperm length dimorphism. The present work is a contribution to the understanding of sperm competition through a comparative study of sperm kinetic parameters in four of these species. Videomicrographic observations at 200 frames per second of sperm from males and females, out of the storage organ, prior or after storage were made. Drosophila sperm display both major and minor waves. The former is analysed by measuring coiling diameter (micron) and the latter by recording both beat frequency (s-1) and wave propagation velocity (micron.s-1). Results show that the 'behaviour' of short and long spermatozoa noticeably differ: short sperm kinetics remains unaltered after storage while both major and minor waves of long spermatozoa are markedly modified. Thus, evidence is provided here of a sort of "differential activation" which is assumed to result in different survival abilities of short and long sperm within the storage organ of females.

Niche separation of African Lissocephala within the Ficus Drosophilid community.

The oviposition sites and larval cycle of the African species of Lissocephala, the most primitive genus of Drosophilidae, are described here for the first time. The genus Lissocephala has achieved a novel adaptive direction in the Ethiopian region. All known African species are strictly specialized on Ficus. This species diversity suggests that ecological transfer to Ficus preceded the Lissocephala radiation. Lissocephala larvae breed inside immature figs. The eggs are laid in or near the fig ostiole. First instar larvae enter the fig receptacle though the ostiolar entrance is constantly closed by firmly imbricating bracts. Third instar larvae leave the fig by crawling out between the ostiolar bracts, and drop to the soil where they pupate. Thus Lissocephala species larvae breed inside a sheltered microhabitat, since the numerous other sympatric sycophagous Drosophilids do not have the ability to colonize immature figs. Other groups of Drosophilid species breed successively on the ripening exocarp of the fig following the successive microbial states of the fig. The possibility of coevolution of Lissocephala species, Ficus species and pollinator fig wasp species is discussed. Selection for avoidance of competition increased Lissocephala species' efficiency in exploiting unutilized immature figs and then provided a conspicuous niche separation which contributed to species packing on figs.