James P. Randerson

The evolutionary dynamics of male‐killers and their hosts

Male-killing bacteria are cytoplasmic sex-ratio distorters that are transmitted vertically through females of their insect hosts. The killing of male hosts by their bacteria is thought to be an adaptive bacterial trait because it augments the fitness of female hosts carrying clonal relatives of those bacteria. Here we attempt to explain observations of multiple male-killers in natural host populations. First we show that such male-killer polymorphism cannot be explained by a classical model of male-killing. We then show that more complicated models incorporating the evolution of resistance in hosts can explain male-killer polymorphism. However, this is only likely if resistance genes are very costly. We also consider the long-term evolutionary dynamics of male-killers, and show that evolution towards progressively more ‘efficient’ male-killers can be thwarted by the appearance of host resistance. The presence of a resistance gene can allow a less efficient male-killer to outcompete its rival and hence reverse the trend towards more efficient transmission and reduced metabolic load on the host.

The uncertain evolution of the sexes

What forces gave rise to the evolution of the size difference between sperm and eggs? For many years, it has been all but accepted wisdom that the answer was laid out by Parker et al. However, their model requires an unusual and unverified assumption regarding the relationship between zygote size and fitness. Although the first phylogenetically controlled test of the comparative predictions of the model is consistent, the results have a simple alternative interpretation. Furthermore, recent work has formalized different theoretical frameworks that require less unusual assumptions. These postulate, for example, that, under sperm limitation, a larger egg will have an increased chance of being fertilized, either because its own mass offers a larger target for sperm or because larger eggs can produce a greater quantity of attraction pheromone. Other frameworks either point to small sperm preventing transmission of cytoplasmic symbionts and/or organelles or having a motility advantage. At present, however, no model is capable of offering a universal explanation.

Male killing can select for male mate choice: a novel solution to the paradox of the lek

In lekking species, intense directional selection is applied to aspects of the male genotype by female choice. Under conventional quantitative genetics theory, the expectation is that this will lead to a rapid loss in additive genetic variance for the trait in question. However, despite female choice, male variation is maintained and hence it pays females to continue choosing. This has been termed the ‘paradox of the lek’. Here we present a theoretical analysis of a putative sex–role–reversed lek in the butterfly Acraea encedon. Sex–role reversal appears to have come about because of infection with a male–killing Wolbachia. The bacterium is highly prevalent in some populations, such that there is a dearth of males. Receptive females form dense aggregations, and it has been suggested that males preferentially select females uninfected with the bacterium. As with more conventional systems, this presents a theoretical problem exactly analogous to the lek paradox, namely, what maintains female variation and hence why do males continue to choose? We model the evolution of a male choice gene that allows discrimination between infected and uninfected females, and show that the stable maintenance of both female variation and male choice is likely, so long as males make mistakes when discriminating between females. Furthermore, our model allows the maintenance, in a panmictic population, of a male killer that is perfectly transmitted. This is the first model to allow this result, and may explain the long–term persistence of a male killer in Hypolimnas bolina.

HOW CAN SEX RATIO DISTORTERS REACH EXTREME PREVALENCES? MALE-KILLING WOLBACHIA ARE NOT SUPPRESSED AND HAVE NEAR-PERFECT VERTICAL TRANSMISSION EFFICIENCY IN ACRAEA ENCEDON

Abstract.— Maternally transmitted bacteria that kill male hosts early in their development are found in many insects. These parasites typically infect 1–30% of wild females, but in a few species of insects, prevalences exceed 95%. We investigated one such case in the butterfly Acraea encedon, which is infected with a male‐killing Wolbachia bacterium. We measured three key parameters that affect the prevalence of the parasite: transmission efficiency, rate of survival of infected males, and the direct cost of infection. We observed that all wild females transmit the bacterium to all their offspring and that all infected males die in wild populations. We were unable to detect any physiological cost to infection in lab culture. These observations explain the high prevalence of the A. encedon male killer, as theory predicts that under these conditions the parasite will spread to fixation. This will occur provided the death of males provides some benefit to the surviving infected females. The problem therefore becomes why the bacterium has not reached fixation and driven the butterfly extinct due to the shortage of males. We therefore investigated whether males choose to mate with uninfected rather than infected females, as this would prevent the bacterium from reaching fixation. We tested this hypothesis in the “lekking swarms” of virgin females found in the most female‐biased populations, and were unable to detect any evidence of mate choice. In conclusion, this male killer has spread to high prevalence because it has a high transmission efficiency and low cost, but the factors maintaining uninfected females in the population remain unknown.

Survival and anisogamy.

Response from Randerson and HurstBulmer et al. [1xSee all References[1] wish to correct an ‘error’ in our model and another in its interpretation. We are grateful for the opportunity that they provide to allow us to expand on a difficulty that we barely touched on previously. With this more fully described, it will be clear that their replacement model is logically inconsistent. However, if their assertion is correct as regards the interpretation of our result, it demonstrates that the field (see e.g. [2.xBulmer, M. See all References, 3.xSelection for high gamete encounter rates explains the success of male and female mating types. Dusenbery, D.B. J. Theor. Biol. 2000; 202: 1–10Crossref | PubMed | Scopus (33)See all References, 4.xMaynard Smith, J. See all References, 5.xThe evolution of sexes. Hoekstra, R.F. : 59–91CrossrefSee all References]), ourselves included [6xThe uncertain evolution of the sexes. Randerson, J.P. and Hurst, L.D. Trends Ecol. Evol. 2001; 16: 571–579Abstract | Full Text | Full Text PDF | Scopus (43)See all References[6], has been concentrating on a red herring for the past 30 years. Although the potential importance of this novel insight should not be understated, it is, however, problematic.Central to both points is the understanding that a biologically reasonable and theoretically consistent model must assume some finite zygote size below which zygote fitness is zero. Suppose that this is not true and that the curve is of the form in their Fig. 1 [1xSee all References[1] (i.e. one that runs through the origin), selection then favours the evolution of isogamy with gametes getting ever smaller: the ESS is a gamete of zero size [2xBulmer, M. See all References[2]. As this is impossible, a minimum gamete size must be evoked [2xBulmer, M. See all References[2]. If there must be a minimum size for gametic viability, it is logically inconsistent and biologically unreasonable to suppose that the same is not true for zygotes.Bulmer et al. note that our attempt to model the relationship between zygote size and fitness relied on an approximation. Their alternative, however, leads to a model that supposes that fitness is zero only if zygote size is zero; that is it requires the above logical inconsistency. Our approximation, by contrast, allows for some finite zygote size existing below which zygote fitness is zero. Which is the least misleading should be open to experimental testing.By far the most important point raised by Bulmer et al., however, is that, if we are correct in supposing a minimum zygote size for viability, the ancient debate [2.xBulmer, M. See all References, 3.xSelection for high gamete encounter rates explains the success of male and female mating types. Dusenbery, D.B. J. Theor. Biol. 2000; 202: 1–10Crossref | PubMed | Scopus (33)See all References, 4.xMaynard Smith, J. See all References, 5.xThe evolution of sexes. Hoekstra, R.F. : 59–91CrossrefSee all References] about the form of curve relating zygote size to fitness is irrelevant. It is typically argued that the PBS argument [7xThe origin and evolution of gamete dimorphism and the male-female phenomenon. Parker, G.A. et al. J. Theor. Biol. 1972; 36: 181–198Crossref | Scopus (229)See all References[7] could only function if the relationship between zygote size and zygote fitness is s shaped. Bulmer et al. now argue that, with a finite minimum zygote size and an increasing but decelerating curve (any form will do), anisogamy will result. Although it would be helpful to see that this result is robust in a population genetical framework (not all game theoretical arguments are, e.g. see [8xTransitions in the evolution of meiosis. Hurst, L.D. and Randerson, J.P. J. Evol. Biol. 2000; 13: 466–479Crossref | Scopus (3)See all References[8]), this greatly expands the theoretical zone within which PBS-like arguments will work.The problem is, however, that all logically consistent conditions appear to lead to anisogamy: for the stable maintenance of isogamy, Bulmer et al. evoke a model in which a finite minimum zygote size is not found (Fig. 17a [4xMaynard Smith, J. See all References[4]). Hence, their assertion that the conditions generating anisogamy become more probable during the transition from uni- to multicellularity is questionable. What might be more important is a transition from a short diploid phase, in which selection on gametic phase is most important, to a long one, in which selection on the zygotic–pre-gametic phase is of more importance. Although a potentially significant assumption has been exposed, the relevance is uncertain.