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Polyandry, female mating with multiple males, is widespread across many taxa and almost ubiquitous in insects. This conflicts with the traditional idea that females are constrained by their comparatively large investment in each offspring, and so should only need to mate once or a few times. Females may need to mate multiply to gain sufficient sperm supplies to maintain their fertility, especially in species in which male promiscuity results in division of their ejaculate among many females. Here, we take a novel approach, utilizing wild‐caught individuals to explore how natural variation among females and males influences fertility gains for females. We studied this in the Malaysian stalk‐eyed fly species Teleopsis dalmanni. After an additional mating, females benefit from greatly increased fertility (proportion fertile eggs). Gains from multiple mating are not uniform across females; they are greatest when females have high fecundity or low fertility. Fertility gains also vary spatially, as we find an additional strong effect of the stream from which females were collected. Responses were unaffected by male mating history (males kept with females or in male‐only groups). Recent male mating may be of lesser importance because males in many species, including T. dalmanni, partition their ejaculate to maintain their fertility over many matings. This study highlights the importance of complementing laboratory studies with data on wild‐caught populations, where there is considerable heterogeneity between individuals. Future research should focus on environmental, demographic and genetic factors that are likely to significantly influence variation in individual female fecundity and fertility.

Background Mitochondria are predominantly inherited from the maternal gamete, even in unicellular organisms. Yet an extraordinary array of mechanisms enforce uniparental inheritance, which implies shifting selection pressures and multiple origins. Results We consider how this high turnover in mechanisms controlling uniparental inheritance arises using a novel evolutionary model in which control of mitochondrial transmission occurs either during spermatogenesis (by paternal nuclear genes) or at/after fertilization (by maternal nuclear genes). The model treats paternal leakage as an evolvable trait. Our evolutionary analysis shows that maternal control consistently favours strict uniparental inheritance with complete exclusion of sperm mitochondria, whereas some degree of paternal leakage of mitochondria is an expected outcome under paternal control. This difference arises because mito-nuclear linkage builds up with maternal control, allowing the greater variance created by asymmetric inheritance to boost the efficiency of purifying selection and bring benefits in the long term. In contrast, under paternal control, mito-nuclear linkage tends to be much weaker, giving greater advantage to the mixing of cytotypes, which improves mean fitness in the short term, even though it imposes a fitness cost to both mating types in the long term. Conclusions Sexual conflict is an inevitable outcome when there is competition between maternal and paternal control of mitochondrial inheritance. If evolution has led to complete uniparental inheritance through maternal control, it creates selective pressure on the paternal nucleus in favour of subversion through paternal leakage, and vice versa. This selective divergence provides a reason for the repeated evolution of novel mechanisms that regulate the transmission of paternal mitochondria, both in the fertilized egg and spermatogenesis. Our analysis suggests that the widespread occurrence of paternal leakage and prevalence of heteroplasmy are natural outcomes of this sexual conflict. Electronic supplementary material The online version of this article (doi:10.1186/s12915-017-0437-8) contains supplementary material, which is available to authorized users.

All too often, studies of sexual selection focus exclusively on the responses in one sex, on single traits, typically those that are exaggerated and strongly sexually dimorphic. They ignore a range of less obvious traits and behavior, in both sexes, involved in the interactions leading to mate choice. To remedy this imbalance, we analyze a textbook example of sexual selection in the stalk‐eyed fly (Diasemopsis meigenii). We studied several traits in a novel, insightful, and efficient experimental design, examining 2,400 male–female pairs in a “round‐robin” array, where each female was tested against multiple males and vice versa. In D. meigenii, females exhibit strong mate preference for males with highly exaggerated eyespan, and so we deliberately constrained variation in male eyespan to reveal the importance of other traits. Males performing more precopulatory behavior were more likely to attempt to mate with females and be accepted by them. However, behavior was not a necessary part of courtship, as it was absent from over almost half the interactions. Males with larger reproductive organs (testes and accessory glands) did not make more mating attempts, but there was a strong tendency for females to accept mating attempts from such males. How females detect differences in male reproductive organ size remains unclear. In addition, females with larger eyespan, an indicator of size and fecundity, attracted more mating attempts from males, but this trait did not alter female acceptance. Genetic variation among males had a strong influence on male mating attempts and female acceptance, both via the traits we studied and other unmeasured attributes. These findings demonstrate the importance of assaying multiple traits in males and females, rather than focusing solely on prominent and exaggerated sexually dimorphic traits. The approach allows a more complete understanding of the complex mating decisions made by both males and females.

Földvári, Mihály, Mikó, István, Ulmer, Jonah M., Rolo, Tomy dos Santos, Csősz, Sándor, Pomiankowski, Andrew, Baumbach, Tilo, Kamp, Thomas van de (2019): Jumping and Grasping: Universal Locking Mechanisms in Insect Legs. Insect Systematics and Diversity (AIFB) 3 (6), No. 3: 1-16, DOI: 10.1093/isd/ixz018, URL: http://dx.doi.org/10.1093/isd/ixz018

Thickened femora of insects are correlated to enlarged muscle masses and serve two basic purposes: jumping/kicking and grasping/holding. Modifications on the ventral femoral wall and the tibial flexor tendon that are possibly involved in catch mechanisms have been described in multiple insect taxa with both jumping and grasping legs. Our comparative study aims to explore the functional and structural similarities of these modification in jumping and grasping leg types from Coleoptera, Hymenoptera, Diptera, and Orthoptera with the combination of cutting edge, noninvasive imaging methods, and classical dissections techniques. Our data indicate that locking mechanisms are present in the jumping and grasping legs of insects. We describe three femoro-tibial lock types based on the location of the interacting sclerites relative to the site of origin of the tibial flexor tendon. All of the three types can be found in jumping insect legs, whereas only one type is present in grasping legs. The locking mechanism might aid in keeping the femoro-tibial joint in a flexed position for an extended period of time. Our data indicate that morphologically similar modifications in the femoro-tibial joint are involved in energy-saving mechanisms both in jumping and grasping legs in insects.

Male mate preferences have been demonstrated across a range of species, including the Malaysian stalk-eyed fly,Teleopsis dalmanni. This species is subject to SR, an X-linked male meiotic driver, that causes the dysfunction of Y-sperm and the production all female broods. SR is associated with a low frequency inversion spanning most of the X chromosome that causes reduced organismal fitness. While there has been work considering female avoidance of meiotic drive males, the mating decisions of drive-bearing males have not been considered previously. As drive males are of lower genetic quality they may be less able to bear the cost of choice or may experience weaker selection for its maintenance if they are avoided by females. We investigated preference of drive males using binary choice trials. We confirmed that males prefer to mate with large females (indicative of greater fecundity) but found no evidence that the strength of male mate preference differs between drive and standard males. This suggests that the cost of choice does not restrict male reference among drive males. In a further experiment, we found that large eyespan males showed strong preference whereas small eyespan males showed no preference. This is likely to weaken mate preference in drive males, as on average they have reduced eyespan compared to standard males. In this respect, drive males are subject to and exert weak sexual selection.Lay summaryWe studied male mate preference in stalk-eyed flies. This species suffers from meiotic drive, a selfish genetic element that causes a reduction in sperm production and organismal fitness. We predicted that males with meiotic drive would show weak mate preference. Males preferred to mate with large females, but there was no difference in the strength of preference between drive and non-drive males. Males with larger eyespan showed stronger mate preference. Meiotic drive males usually have reduced eyespan so on average they exert weaker sexual selection on females, but this is mediated by eyespan, not genotypeper se.

SR meiotic drive is a selfish genetic element located on the X chromosome in a number of species that causes dysfunction of Y-bearing sperm. SR is transmitted to up to 100% of offspring, causing extreme sex ratio bias. SR in several species is found in a stable polymorphism at a moderate frequency, suggesting there must be strong frequency-dependent selection resisting its spread. We investigate the effect of SR on female and male egg-to-adult viability in the Malaysian stalk-eyed fly,Teleopsis dalmanni. SR meiotic drive in this species is old, and appears to be broadly stable at a moderate (~20%) frequency. We use large-scale controlled crosses to estimate the strength of selection acting against SR in female and male carriers. We find that SR reduces the egg-to-adult viability of both sexes. In females, homozygous females experience greater reduction in viability (sf= 0.242) and the deleterious effects of SR are additive (ℎ = 0.511). The male deficit in viability (sm= 0.214) is not different from that in homozygous females. The evidence does not support the expectation that deleterious side-effects of SR are recessive or sex-limited. We discuss how these reductions in egg-to-adult survival, as well as other forms of selection acting on SR, act to maintain SR polymorphism in this species.

There is considerable debate over the value of male sexual ornaments as signals of genetic quality. Studies alternately report that environmental variation enhances or diminishes the genetic signal, or leads to crossover where genotypes perform well in one environment but poorly in another. A unified understanding is lacking. We conduct the first experimental test examining the dual effects of distinct low and high genetic quality (inbred versus crossed parental lines) and low, through high, to extreme environmental stress (larval diets) on a condition-dependent male ornament. We find that differences in genetic quality signalled by the ornament (male eyespan inDiasemopsis meigeniistalk-eyed flies) become visible and are amplified under high stress but are overwhelmed in extreme stress environments. Variance among distinct genetic lines increases with environmental stress in both genetic quality classes, but at a slower rate in high quality outcrossed flies. Individual genetic lines generally maintain their ranks across environments, except among high quality lines under low stress conditions, where low genetic variance precludes differentiation between ranks. Our results provide a conceptual advance, demonstrating a unified pattern for how genetic and environmental quality interact. They show when environmental conditions lead to the amplification of differences in signals of genetic quality and thereby enhance the potential indirect genetic benefits gained by female mate choice.

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