Nutrient-dependent allometric plasticity in a male-diphenic mite.

Male secondary sexual traits often scale allometrically with body size. These allometries can be variable within species and may shift depending on environmental conditions, such as food quality. Such allometric plasticity has been hypothesized to initiate local adaptation and evolutionary diversification of scaling relationships, but is under-recorded, and its eco-evolutionary effects are not well understood. Here, we tested for allometric plasticity in the bulb mite (Rhizoglyphus robini), in which large males tend to develop as armed adult fighters with thickened third legs, while small males become adult scramblers without thickened legs. We first examined the ontogenetic timing for size- and growth-dependent male morph determination, using experimentally amplified fluctuations in growth rate throughout juvenile development. Having established that somatic growth and body size determine male morph expression immediately before metamorphosis, we examined whether the relationship between adult male morph and size at metamorphosis shifts with food quality. We found that the threshold body size for male morph expression shifts toward lower values with deteriorating food quality, confirming food-dependent allometric plasticity. Such allometric plasticity may allow populations to track prevailing nutritional conditions, potentially facilitating rapid evolution of allometric scaling relationships.

Cross-level considerations for explaining selection pressures and the maintenance of genetic variation in condition-dependent male morphs.

Condition-dependent expression of alternative male morphologies (AMMs) exists in many arthropods. Understanding their coexistence requires answering (at least) two questions: (i) what are the ecological selection pressures that maintain condition-dependent plasticity of AMM expression, and (ii) what maintains the associated genetic variation? Focusing on acarid mites, we show that the questions should not be conflated. We argue how, instead, answers should be sought by testing phenotype-level (question 1) or genotype-level (question 2) hypotheses. We illustrate that energy allocation restrictions and physiological trade-offs are likely to play a crucial role in AMM expression in acarid mites. We thus conclude that these aspects require specific attention in identifying selection pressures maintaining condition-dependent plasticity, and evolutionary processes that maintain genetic variation in condition-dependent phenotypic plasticity.

Repeated evolution of asymmetric genitalia and right-sided mating behavior in the Drosophila nannoptera species group.

BACKGROUND: Male genitals have repeatedly evolved left-right asymmetries, and the causes of such evolution remain unclear. The Drosophila nannoptera group contains four species, among which three exhibit left-right asymmetries of distinct genital organs. In the most studied species, Drosophila pachea, males display asymmetric genital lobes and they mate right-sided on top of the female. Copulation position of the other species is unknown. RESULTS: To assess whether the evolution of genital asymmetry could be linked to the evolution of one-sided mating, we examined phallus morphology and copulation position in D. pachea and closely related species. The phallus was found to be symmetric in all investigated species except D. pachea, which displays an asymmetric phallus with a right-sided gonopore, and D. acanthoptera, which harbors an asymmetrically bent phallus. In all examined species, males were found to position themselves symmetrically on top of the female, except in D. pachea and D. nannoptera, where males mated right-sided, in distinctive, species-specific positions. In addition, the copulation duration was found to be increased in the nannoptera group species compared to closely related outgroup species. CONCLUSION: Our study shows that gains, and possibly losses, of asymmetry in genital morphology and mating position have evolved repeatedly in the nannoptera group. Current data does not allow us to conclude whether genital asymmetry has evolved in response to changes in mating position, or vice versa.

Drosophila pachea asymmetric lobes are part of a grasping device and stabilize one-sided mating.

BACKGROUND: Multiple animal species exhibit morphological asymmetries in male genitalia. In insects, left-right genital asymmetries evolved many times independently and have been proposed to appear in response to changes in mating position. However, little is known about the relationship between mating position and the interaction of male and female genitalia during mating, and functional analyses of asymmetric morphologies in genitalia are virtually non-existent. We investigated the relationship between mating position, asymmetric genital morphology and genital coupling in the fruit fly Drosophila pachea, in which males possess an asymmetric pair of external genital lobes and mate in an unusual right-sided position on top of the female. RESULTS: We examined D. pachea copulation by video recording and by scanning electron microscopy of genital complexes. We observed that the interlocking of male and female genital organs in D. pachea is remarkably different from genital coupling in the well-studied D. melanogaster. In D. pachea, the female oviscapt valves are asymmetrically twisted during copulation. The male's asymmetric lobes tightly grasp the female's abdomen in an asymmetric 'locking' position, with the left and right lobes contacting different female structures. The male anal plates, which grasp the female genitalia in D. melanogaster, do not contact the female in D. pachea. Experimental lobe amputation by micro-surgery and laser-ablation of lobe bristles led to aberrant coupling of genitalia and variable mating positions, in which the male was tilted towards the right side of the female. CONCLUSION: We describe, for the first time, how the mating position depends on coupling of male and female genitalia in a species with asymmetric genitalia and one-sided mating position. Our results show that D. pachea asymmetric epandrial lobes do not act as a compensatory mechanism for the change from symmetric to one-sided mating position that occurred during evolution of D. pachea's ancestors, but as holding devices with distinct specialized functions on the left and right sides.