170 Years of “Lock-and-Key”: Genital Morphology and Reproductive Isolation

The divergent genital morphology observed among closely related animal species has long been posited as a mechanism of reproductive isolation. Despite the intuitive appeal that rapidly evolving genitalia might cause speciation, evidence for its importance—or even its potential—in reproductive isolation is mixed. Most tests of genital structural isolation between species often fail to find convincing evidence that differences in morphology prevent copulation or insemination between species. However, recent work suggests that differences in genital morphology might contribute to reproductive isolation in less obvious ways through interactions with sensory mechanisms that result in lowered reproductive fitness in heterospecific matings. In this paper, I present a brief history of the “lock-and-key” hypothesis, summarize the evidence for the involvement of genital morphology in different mechanisms of reproductive isolation, discuss progress in identifying the molecular and genetic bases of species differences in genital morphology, and discuss prospects for future work on the role of genitalia in speciation

A Sex-Ratio Meiotic Drive System in Drosophila Simulans. I: An Autosomal Suppressor

Sex ratio distortion (sex-ratio for short) has been reported in numerous species such as Drosophila, where distortion can readily be detected in experimental crosses, but the molecular mechanisms remain elusive. Here we characterize an autosomal sex-ratio suppressor from D. simulans that we designate as not much yang (nmy, polytene chromosome position 87F3). Nmy suppresses an X-linked sex-ratio distorter, contains a pair of near-perfect inverted repeats of 345 bp, and evidently originated through retrotransposition from the distorter itself. The suppression is likely mediated by sequence homology between the suppressor and distorter. The strength of sex-ratio is greatly enhanced by lower temperature. This temperature sensitivity was used to assign the sex-ratio etiology to the maturation process of the Y-bearing sperm, a hypothesis corroborated by both light microscope observations and ultrastructural studies. It has long been suggested that an X-linked sex-ratio distorter can evolve by exploiting loopholes in the meiotic machinery for its own transmission advantage, which may be offset by other changes in the genome that control the selfish distorter. Data obtained in this study help to understand this evolutionary mechanism in molecular detail and provide insight regarding its evolutionary impact on genomic architecture and speciation.Organismic and Evolutionary Biolog

Molecular Divergence with Major Morphological Consequences: Development and Evolution of Organ Size and Shape

Understanding the causes of the morphological diversity among organisms is a topic of great interest to evolutionary developmental biologists. Although developmental biologists have had great success in identifying the developmental mechanisms and molecular processes that specify organ size and shape within species, only relatively recently have the molecular tools become available to study how variation in these mechanisms gives rise to the phenotypic differences that are observed among closely related species. In addition to these technological advances, researchers interested in understanding how molecular variation gives rise to phenotypic variation have used three primary strategies to identify the molecular differences underlying species-specific traits: the candidate gene approach, differential gene expression screens, and between-species genetic mapping experiments. In this review, we discuss how these approaches have been successful in identifying the genes and the cellular mechanisms by which they specify variation in one of the most recognizable examples of the evolution of organ size, the adaptive variation in beak morphology among Darwin’s finches. We also discuss insect reproductive structures as a model with great potential to advance our understanding of the specification and evolution of organ size and shape differences among species. The results from these two examples, and those from other species, show that species-specific variation in organ size and shape typically evolves via changes in the timing, location, and amount of gene/protein expression that act on tissue growth processes.YesThis is the accepted manuscript version of the following article: Masly, J. & Azom, M. (2022). Molecular divergence with major morphological consequences: Development and evolution of organ size and shape. Essays in Biochemistry, 66 (6). https://doi.org/10.1042/EBC20220118

High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila

Postzygotic reproductive isolation is characterized by two striking empirical patterns. The first is Haldane's rule—the preferential inviability or sterility of species hybrids of the heterogametic (XY) sex. The second is the so-called large X effect—substitution of one species's X chromosome for another's has a disproportionately large effect on hybrid fitness compared to similar substitution of an autosome. Although the first rule has been well-established, the second rule remains controversial. Here, we dissect the genetic causes of these two rules using a genome-wide introgression analysis of Drosophila mauritiana chromosome segments in an otherwise D. sechellia genetic background. We find that recessive hybrid incompatibilities outnumber dominant ones and that hybrid male steriles outnumber all other types of incompatibility, consistent with the dominance and faster-male theories of Haldane's rule, respectively. We also find that, although X-linked and autosomal introgressions are of similar size, most X-linked introgressions cause hybrid male sterility (60%) whereas few autosomal introgressions do (18%). Our results thus confirm the large X effect and identify its proximate cause: incompatibilities causing hybrid male sterility have a higher density on the X chromosome than on the autosomes. We evaluate several hypotheses for the evolutionary cause of this excess of X-linked hybrid male sterility

Data from: Asymmetric mismatch in strain-specific genital morphology causes increased harm to Drosophila females

Although several evolutionary forces have been proposed to contribute to genital morphological diversification, it is unclear which might act early during the evolution of novel structural traits. We test the hypothesis that mismatch between interacting male and female secondary sexual structures gives rise to increased harm to females, consistent with the outcome predicted from a history of sexual conflict. We mate Drosophila sechellia females to males from a collection of D. mauritiana-D. sechellia interspecific genetic introgression lines that possess quantitative morphological variation in the posterior lobe of the genital arch, an external genital structure that can cause wounds to the female abdomen during mating. We find that males with smaller posterior lobes, and those that possess lobes with similarities in shape to D. mauritiana, cause more severe wounding compared to either D. sechellia males with strain-specific morphologies or introgression males that possess larger lobes or lobes with more pronounced D. sechellia features. These results suggest a possible history of sexual conflict during the evolution of the posterior lobe in D. sechellia, but also suggest a potential contribution of divergence in sensory recognition mechanisms to posterior lobe evolution

Movie S2

Movie file that shows courtship and copulation behavior of a Uas-Dcr-2; apGAL4; UAS-PoxnIR/elavGAL80 male mated with a white-eyed female

Data from: Multiple sexual selection pressures drive the rapid evolution of complex morphology in a male secondary genital structure

The genitalia of internally fertilizing taxa represent a striking example of rapid morphological evolution. Although sexual selection can shape variation in genital morphology, it has been difficult to test whether multiple sexual selection pressures combine to drive the rapid evolution of individual genital structures. Here, we test the hypothesis that both pre- and postcopulatory sexual selection can act in concert to shape complex structural variation in secondary genital morphology. We genetically modified the size and shape of the posterior lobes of Drosophila melanogaster males and tested the consequences of morphological variation on several reproductive measures. We found that the posterior lobes are necessary for genital coupling and that they are also the targets of multiple postcopulatory processes that shape quantitative variation in morphology, even though these structures make no direct contact with the external female genitalia or internal reproductive organs during mating. We also found that males with smaller and less structurally complex posterior lobes suffer substantial fitness costs in competitive fertilization experiments. Our results show that sexual selection mechanisms can combine to shape the morphology of a single genital structure and that the posterior lobes of D. melanogaster are the targets of multiple postcopulatory selection pressures

Data from: Divergence in female damselfly sensory structures is consistent with a species recognition function but shows no evidence of reproductive character displacement

Males and females transmit and receive signals prior to mating that convey information such as sex, species identity, or individual condition. In some animals, tactile signals relayed during physical contact between males and females before and during mating appear to be important for mate choice or reproductive isolation. This is common among odonates, when a male grasps a female’s thorax with his terminal appendages prior to copulation, and the female subsequently controls whether copulation occurs by bending her abdomen to complete intromission. It has been hypothesized that mechanosensory sensilla on the female thoracic plates mediate mating decisions, but is has been difficult to test this idea. Here, we use North American damselflies in the genus Enallagma (Odonata: Coenagrionidae) to test the hypothesis that variation in female sensilla traits is important for species recognition. Enallagma anna and E. carunculatum hybridize in nature, but experience strong reproductive isolation as a consequence of divergence in male terminal appendage morphology. We quantified several mechanosensory sensilla phenotypes on the female thorax among multiple populations of both species and compared divergence in these traits in sympatry versus allopatry. Although these species differed in features of sensilla distribution within the thoracic plates, we found no strong evidence of reproductive character displacement among the sensilla traits we measured in regions of sympatry. Our results suggest that species‐specific placement of female mechanoreceptors may be sufficient for species recognition, although other female sensory phenotypes might have diverged in sympatry to reduce interspecific hybridization

Wounding data

Tab-delimited text file with wounding measures and associated data