. "Assortative fertilization in Drosophilia." (NAS Colloquium) Genetics and the Origin of Species: From Darwin to Molecular Biology 60 Years After Dobzhansky. Washington, DC: The National Academies Press, 1997.
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Proceedings of the National Academy of Sciences of the United States of America
a small number of inseminations of Drosophila pulchrella females by Drosophila suzukii males. While the numbers of sperm stored in the females appeared to be lower than in either conspecific cross, presumably due to the shorter duration of interspecific copulations, the viability of these sperm was elegantly demonstrated by stimulating their use with injected accessory gland products of conspecific males (7).
In many Drosophila species, primarily of the quinaria and repleta groups, homospecific mating normally is followed by the formation of a large opaque mass in the vagina, the insemination reaction, that typically lasts for 7 to 9 hr (8). Its disappearance is coincident with the onset of oviposition and subsequent remating by the female (9). In heterospecific matings this mass usually lasts considerably longer, and judging from the observations summarized by Patterson and Stone (8), and the phylogenetic relationships (10) of the species they examined, the size and duration of the mass appears to be related to the degree of divergence between the species involved. Patterson and co-workers suggested that this insemination reaction functions as an isolating mechanism, because in some crosses, they observed dead sperm within the mass and, in extreme cases, heterospecifically mated females never remated.
These examples all involve single heterospecific matings. In two other groups of insects, flour beetles (11, 12) and crickets (13–16), positive assortative fertilization was observed only under conditions of double matings, matings involving both a homo- and a heterospecific male. Heterospecific matings, both in floor beetles and in crickets, result in the production of offspring, although in all cases except crosses involving one type of Tribolium female, T. freemani, the numbers of offspring are significantly lower than in conspecific matings. When females are mated, twice, to a heterospecific and to a homospecific male, regardless of mating order, a significant majority of the offspring were sired by males of their own species. In both cases, positive assortative fertilization is the outcome of interejaculate competition dependent upon female genotype. Most of the progeny produced, regardless of mating order, were sired by the conspecific male. Because in most of these combinations, there were reduced numbers or viability of interspecific sperm after transfer, the observed effect is likely to have resulted merely from a numerical swamping out by the viable and conspecific sperm. This is not likely to be the case in T. freemani females, where sperm of both types of males appear equally viable.
Assortative mating, so pronounced between true species, is often examined in detail among distinct populations of the same species to identify antecedents of speciation. The same approach can be employed in treating assortative fertilization. Assortative fertilization within a species can potentially occur when a female has mated to only one male or when she has multiple mates, as seen for interspecific matings. In Drosophila, I could find no examples of positive assortative fertilization involving either single or multiple homospecific matings. This does not mean that they do not exist.
There are, however, sperm utilization patterns that clearly appear to exemplify negative assortative fertilization. Widely known in plants, the possibility of self-incompatibility in animals has received little attention. There is some evidence, such as increased recurrent spontaneous abortion among couples sharing HLA haplotypes (17), that similarities with respect to major histocompatibility complex variation may influence fertilization or implantation success, but this is poorly defined.
Investigators working with cactophilic Drosophila have long been aware that, compared with Drosophila melanogaster, it is very difficult to create isofemale lines of these species. Markow (18), in a study of inbreeding, reported the existence of a self-sterility phenomenon in Drosophila mojavensis, revealed when sib-mated lines failed to reproduce. Females mated to their brothers were full of motile sperm, and mature ovarian oocytes, but did not oviposit. The viability of these sperm was demonstrated when they were rescued from the ventral receptacles by the sperm-free ejaculates of unrelated males. The fact that these sperm could be “rescued” suggests that the responsible mechanism is a function of nonsperm ejaculate components and their interaction with females. Further analysis has been precluded by the absence of genetically marked chromosome balancers in this species.
A similar phenomenon appears to exist in at least one other species of desert Drosophila. Drosophila nigrospiracula is a cactophilic species in which females will remate up to four times in a given morning. As with D. mojavensis, unless a female is confined with more than one of her brothers (R.L. Mangan, personal communication), attempts to inbreed this species result in most sib-mated lines failing within a few generations (T.A.M., S.Bertram, and S.Murphy, unpublished results). Dissection of adults reveals that parents are fully capable of mating and sperm transfer: in most nonreproductive pairs, females contain large numbers of motile sperm in their ventral receptacles. For some reason, however, these sperm are not being used.
Experiments were conducted to assess whether the males or females were, for some unapparent reason, sterile, and if not, whether, as with D. mojavensis, degree of relatedness acts to prevent sperm utilization. In one set of experiments, oviposition was compared between females mated once to a brother following one generation of sib mating, and females mated to a random male. There was no difference in copulation duration for females mated to sibs compared with random males. In both replications, two things are clear (Table 1). First, fewer females laid any eggs when mated to their brothers than did females mated to random males. Second, those females that did not oviposit did not fail to do so for lack of motile sperm. A high proportion of females did not utilize the sperm they carried, at least from a single mating.
In the second experiment, females were mated three times in the same morning. Matings were either all to the same male, “random” or “sib” (a brother from a one-generation sib-mated line), or twice consecutively to a sib and then to a random male from the population (Table 1). In both replications, a mating to an unrelated male was associated with increased oviposition, suggesting that degree of relatedness is an important factor in determining whether females of this species give up their
Table 1. Reproductive failure and sperm presence in inbred and random pair matings of D. nigrospiracla
No. of females
Females not ovipositing
Females with sperm
Females in experiments 1×a and 1×b were mated once, to either a male chosen at random from the mass mating culture or to their brother after one generation of sib-mating. Females in experiments 3×a and 3×b were mated three times, either all three times to the same male, a brother, or twice to their brother and then to a male chosen at random from the mass culture. All matings were observed to ensure normal copulations were achieved. Mated females were separated from males and allowed to lay eggs in yeasted vials, changed daily, for 1 week. Females not ovipositing after 1 week were dissected and examined for the presence of motile sperm.