Rapid divergent evolution of internal female genitalia and the coevolution of male genital morphology revealed by micro-computed tomography.

Animal genitalia are thought to evolve rapidly and divergently in response to sexual selection. Studies of genital evolution have focused largely on male genitalia. The paucity of work on female genital morphology is probably due to problems faced in quantifying shape variation, due to their composition and accessibility. Here we use a combination of micro-computed tomography, landmark free shape quantification and phylogenetic analysis to quantify the rate of female genital shape evolution among 29 species of Antichiropus millipedes, and their coevolution with male genitalia. We found significant variation in female and male genital shape among species. Male genital shape showed a stronger phylogenetic signal than female genital shape, although the phylogenetic signal effect sizes did not differ significantly. Male genital shape was found to be evolving 1.2 times faster than female genital shape. Female and male genital shape exhibited strong correlated evolution, indicating that genital shape changes in one sex are associated with corresponding changes in the genital shape of the other sex. This study adds novel insight into our growing understanding of how female genitalia can evolve rapidly and divergently, and highlights the advantages of three-dimensional techniques and multivariate analyses in studies of female genital evolution.

Sexual Selection Shapes Seminal Vesicle Secretion Gene Expression in House Mice.

Reproductive proteins typically have high rates of molecular evolution, and are assumed to be under positive selection from sperm competition and cryptic female choice. However, ascribing evolutionary divergence in the genome to these processes of sexual selection from patterns of association alone is problematic. Here, we use an experimental manipulation of postmating sexual selection acting on populations of house mice and explore its consequences for the expression of seminal vesicle secreted (SVS) proteins. Following 25 generations of selection, males from populations subjected to postmating sexual selection had evolved increased expression of at least two SVS genes that exhibit the signature of positive selection at the molecular level, SVS1 and SVS2. These proteins contribute to mating plug formation and sperm survival in the female reproductive tract. Our data thereby support the view that sexual selection is responsible for the evolution of these seminal fluid proteins.

The evolution of female genitalia.

Female genitalia have been largely neglected in studies of genital evolution, perhaps due to the long-standing belief that they are relatively invariable and therefore taxonomically and evolutionarily uninformative in comparison with male genitalia. Contemporary studies of genital evolution have begun to dispute this view, and to demonstrate that female genitalia can be highly diverse and covary with the genitalia of males. Here, we examine evidence for three mechanisms of genital evolution in females: species isolating 'lock-and-key' evolution, cryptic female choice and sexual conflict. Lock-and-key genital evolution has been thought to be relatively unimportant; however, we present cases that show how species isolation may well play a role in the evolution of female genitalia. Much support for female genital evolution via sexual conflict comes from studies of both invertebrate and vertebrate species; however, the effects of sexual conflict can be difficult to distinguish from models of cryptic female choice that focus on putative benefits of choice for females. We offer potential solutions to alleviate this issue. Finally, we offer directions for future studies in order to expand and refine our knowledge surrounding female genital evolution.

Social manipulation of sperm competition intensity reduces seminal fluid gene expression.

A considerable body of evidence supports the prediction that males should increase their expenditure on the ejaculate in response to sperm competition risk. The prediction that they should reduce their expenditure with increasing sperm competition intensity is less well supported. Moreover, most studies have documented plasticity in sperm numbers. Here we show that male crickets Teleogryllus oceanicus exhibit reduced seminal fluid gene expression and accessory gland mass in response to elevated sperm competition intensity. Together with previous research, our findings suggest that strategic adjustments in seminal fluid composition contribute to competitive fertilization success in this species.

Divergence in the internal genital morphology of females and correlated divergence in male intromittent structures among populations of a millipede.

Our understanding of genital evolution comes largely from studies of male genitalia. Females have received far less attention because of the difficulties inherent in quantifying the shapes of their internal genital structures. Here we combine advances in micro-computed tomography with a new landmark free method of quantifying three-dimensional trait shape, to document patterns of divergence in female genital shape, and the correlated divergence of male genitalia among populations of the millipede Antichiropus variabilis. We used single-nucleotide polymorphisms to estimate levels of neutral genetic divergence among seven populations of millipede. Genetic divergence was high and correlated with geographic distance. Comparing phenotypic divergence in genital shape to neutral genetic divergence, we found that genital shape for both females and males has diverged more than would be expected from random drift, consistent with a pattern of directional selection. While there was significant covariation between female and male genital shape across populations, the magnitude of divergence in genital shape between the sexes was not correlated. Our results demonstrate the utility of using three-dimensional scanning technologies to examine female genital traits and add to a small but growing number of studies showing that like male genitalia, female genitalia can be under strong directional selection.

Female genitalia.

In this Quick guide, Nadia Sloan and Leigh Simmons introduce the diverse and fascinating biology of female genitalia.

Male-biased sex ratio does not promote increased sperm competitiveness in the seed beetle, Callosobruchus maculatus.

Sperm competition risk and intensity can select for adaptations that increase male fertilisation success. Evolutionary responses are examined typically by generating increased strength of sexual selection via direct manipulation of female mating rates (by enforcing monandry or polyandry) or by alteration of adult sex ratios. Despite being a model species for sexual selection research, the effect of sexual selection intensity via adult sex-ratio manipulation on male investment strategies has not been investigated in the seed beetle, Callosobruchus maculatus. We imposed 32 generations of experimental evolution on 10 populations of beetles by manipulating adult sex ratio. Contrary to predictions, males evolving in male-biased populations did not increase their testes and accessory gland size. This absence of divergence in ejaculate investment was also reflected in the fact that males from male-biased populations were not more successful in either preventing females from remating, or in competing directly for fertilisations. These populations already demonstrate divergence in mating behaviour and immunity, suggesting sufficient generations have passed to allow divergence in physiological and behavioural traits. We propose several explanations for the absence of divergence in sperm competitiveness among our populations and the pitfalls of using sex ratio manipulation to assess evolutionary responses to sexual selection intensity.