Strategies of Sexual Reproduction in Aphids

Abstract

Second copulas of Uroleucon cirsii (L.) are shorter on average than first copulas both for individual males and females. This suggests that male aphids are limited by sperm, on the one hand, and that the capacity of females to store sperm is not unlimited. The latter could be the case if sperm from previous copulas was not displaced. In agreement with this, aphid sperm seems to be transmitted in co-operating bundles with the sperm-heads sticking together and the flagella beating synchronously.A male should leave a female when the gain rate in fertilised eggs has dropped to the average gain rate for the habitat. This marginal value theorem was applied to field colonies of the pine needle aphid Schizolachnus obscurus Börner with one and two males respectively. While the search time was higher in colonies with two males, the copula duration was similar. The difference in copula duration predicted from the marginal value model, however, was very small suggesting that it could not be detected in the "noisy" field data. Nevertheless, the average post-copula lasted twice as long in colonies with two males as in colonies with one male. This was due to a higher frequency of prolonged post-copula association and a lower frequency of simply dismounting in colonies with two males suggesting that male S. obscurus are more likely to guard females in the presence of competitors.Aphid species with males that guard each female after copulation can be expected to have less female-biased sex ratios than those with males that only guard infrequently or not at all. This hypothesis has been found to be true for the mate-guarding Euceraphis betulae Koch and the non-guarding Uroleucon cichorii (Koch). This suggests that a transition from non-guarding towards guarding aphids should take place between sex ratios of 13 and 2.5 females per male. If this was true, species with more female-biased sex ratios should not guard, whereas species with less female-biased sex ratios should guard or coulate for longer than is necessary for fertilisation.Asymmetries in kin competition among males or females select for biased sex ratios. Within this overall sex ratio, individuals should allocate their resources differentially to daughters and sons according to their differing conditions and returns in fitness for each offspring sex. These differential sex ratios have been analysed for two aphid species suggesting that kin competition among males prevails in Uroleucon cirsii (L.), but that kin competition among females prevails in Rhopalosiphum padi (L.). This is also plausible, because the life-cycle of R. padi effectively prevents kin competition among males through their migration but not resource competition among related females.Population density experienced by the mothers of the sexual generation of U. cirsii as adults or nymphs did not affect the sex ratio. Differences experienced by the grandmothers, however, did affect the sex ratio. This confirms the hypotheses that sex allocation takes place in the parthenogenetic grandmothers of the sexual generation, because an aphid begins to develop at a time when its parthenogenetic mother is itself still an embryo (telescoping of generations). Nevertheless, a methodological pitfall leading to pseudo-replication still needs to be tackled.Sexual reproduction accelerates the rate of evolutionary changebecause advantageous mutations do not need to occur one after another in the same lineage; and it purges the gene pool of deleterious mutations by occasionally recombining them into non-viable offspring. Despite these long-term advantages of sex, genes causing ameiotic parthenogenesis should gain a two-fold representation in the next generation. This raises two questions: 1) Why has sexual reproduction been maintained in the majority of animal and plant species, despite a two-fold immediate advantage to genes in an asexual competitor? 2) What has kept a few ancient asexual taxa, such as the bdelloid rotifers from extinction, despite the long-term disadvantages of evolutionary inflexibility and mutation accumulation? Through recombination, any germ-line replicator will end up together with a particular mutation at another position in the genome in only half of the gametes produced. That is twice as good as in asexual lineages. At the same time, transposition of functional operons can in principle avoid the detriment of mutation accumulation. Such a "fluid" and modular genome can be seen as a dynamic state between the establishment of new functional copies of genes and their destruction through mutation. Thus, the jumping gene"s perspective might deliver one answer to two important questions of current evolutionary theory.