An organism is said to be sexually dimorphic when male and female conspecifics have anatomical differences in features such as body size, coloration, or ornamentation, but disregarding differences of reproductive organs. Sexual dimorphism is usually a product of sexual selection, with female choice leading to elaborate male ornamentation (e.g., tails of male peacocks) and male-male competition leading to the development of competitive weaponry (e.g., antlers on male moose). However, evolutionary selection also acts on the sensory systems that receivers use to perceive external stimuli. If the benefits of perception to one sex or the other are different, sex differences in sensory systems can arise. For example, female production of signals used to attract mates can put selective pressure on males to improve their ability to detect those signals. As a result, only males of this species will evolve specialized mechanisms to aid in detection of the female signal. This article uses examples of sex differences in the olfactory, visual, and auditory systems Narins, P. and R. Capranica. 1976. Sexual differences in the auditory system of the tree frog Eleutherodactylus coqui. Science, 192:378-380. of various organisms to show how sex differences in sensory systems arise when it benefits one sex and not the other to have enhanced perception of certain external stimuli. In each case, the form of the sex difference reflects the function it serves in terms of enhanced reproductive success.
Sphinx moth olfactory system Male sphinx moths, Manduca sexta, rely on female released sex-pheromones to guide typical zig-zagging flight behaviors used to locate mates.Schneiderman, A.M., Hildebrand, J.G., Brennan, M.M., Tumlinson, J.H. 1986. Transsexually grafted antennae alter pheromone-directed behavior in a moth. Nature, 323:801-803. Although both males and females respond to host plant olfactory cues to locate food sources, detection of and response to sex-pheromones appears to be male specific. Males that are better at detecting female sex-pheromones are able to find signaling females faster, providing them with a reproductive advantage. Since females gain no such advantage for having olfactory systems that are more sensitive to pheromones, enhanced pheromone detection has evolved only in the olfactory system of male M. sexta. The three main sex differences are as follows:
1) Male antennae are enlarged and contain elongated sensilla (sensory organules) not present in females. The pheromone elicits a male response by stimulating male specific receptor cells on a large number of these sensilla, which are located on the antennal flagellum.Sanes, J.R., and Hildebrand J.G. 1976. Structure and development of antennae in a moth, Manduca sexta. Devel. Biol., 51:282-299. The sexually dimorphic sensilla are called male specific type-1 trichoid sensilla, a type of hair-like olfactory sensilla. In contrast, the flagella of female antennae lack these trichoid sensilla projections that make the male antennae appear to be larger and more feather-like. Each trichoid sensilla is innervated by two male specific olfactory receptor cells, with each cell being tuned (most sensitive) to one of two major chemical components of the pheromone.<Kaissling, K-E, Hildebrand, J.G., and Tumlinson, J.H. 1989. Pheromone receptor cells in the male moth Manduca sexta. Arch. Insect Biochem. Physiol. 10:273-279. By evolving larger, pheromone-specific receptors in the peripheral olfactory system, male M. sexta have an improved sensitivity to female pheromones that enhances mate detection.
2) There is also a sex difference in the neural basis of pheromone detection. In a number of insect species, first order olfactory processing centers in the neuropil of the antennal lobe contain a structure called the macroglomerulus in males.Boeckh, J. and Boeckh, V. 1979. Threshold and odor specificity of pheromone-sensitive neurons in the deutocerebrum of Anteraea pernyi and A. polyphemus (Saturnidae). J. Comp. Physiol., 132:235-242.< Matsumoto, S.G., and Hildebrand, J.G. 1981. Olfactory mechanisms in the moth Manduca sexta:Response characteristics and morphology of central neurons in the antennal lobes. Proc. Soc. Lond. B, 213:249-277. Such a structure, called the macroglomerular complex in this species, has been identified in the antennal lobe of M. sexta, and it has been discovered that axons from the male specific olfactory receptor cells found in trichoid sensilla project exclusively to the macroglomerular complex.< Kanzaki, R., Arbas, E.A., Strausfeld, N.J., and Hildebrand, J.G. 1989. Physiology and morphology of projection neurons in the antennal lobe of the male moth Manduca sexta. J. Comp. Physiol. 165:427-454.Christensen, T.A., Hildebrand, J.G. 1987. Male-specific, sex pheromone-selective projection neurons in the antennal lobes of the moth Manduca sexta. J. Comp. Physiol. A., 160:552:569. Further, all the antennal lobe neurons which respond to sex pheromone also have arborizations to the macroglomerular complex, providing more evidence that it plays a key role in the processing of pheromone sensory information in males.
3) Lastly, there is evidence that the male antennal lobe contains male-specific macroglomerular complex projection neurons that relay pheromone information to higher brain structures in the protocerebrum. Since males have significantly larger populations of medial group antennal lobe neurons, it is thought that some of these extra neurons may belong to this male-specific class.Homberg, U., Montague, R.A., Hildebrand, J.G. 1988. Anatomy of antenno-cerebral pathways in the brain of the sphinx month Manduca sexta. Cell Tissue Res., 254:225-281. Kanzaki et al. have since characterized the responses and structures of some of these projection neurons, and have found that projection neurons with dendritic arborizations in the macroglomerular complex and ordinary glomeruli were excited or inhibited by different stimuli (pheromonal vs. non-pheromonal stimuli respectively). These selective response properties indicate that a specialized role in relaying pheromone information is likely.
The male-specific features listed above, found at the levels of primary detection and neural processing in M. sexta, demonstrate how males of this species have evolved sex differences in the sensory system that improve their ability to detect and locate females.
Visual system of flies Sex differences in the visual system of flies are extremely common, with males generally possessing specialized eye features.Kirschfeld, K., Wenk, P. 1976. The dorsal compound eye of simuliid flies: An eye specialized for the detection of small, rapidly moving objects. Z. Naturforsch, 31c:764-765. Flies in the family Bibionidae display a particularly notable dimorphism, with males possessing large dorsal eyes that are absent in females. Female eyes and the ventral eyes of males are very similar, however, suggesting that the male dorsal eyes serve some extra sex specific function. Research on visually guided behavior in flies suggests that male dorsal eyes may be specialized for the detection and capture of females, for which there is a great deal of competition among males.Land, F.M., Collett, T.S. 1975. Visual control of flight behavior in the hoverfly, Syritta pipiens. J. Comp. Physiol., 99:1-66.Land, F.M., Collett, T.S. 1974. Chasing behavior in house flies (Fannia canicularis). J. Comp. Physiol., 89:331-357. Work by Jochen Zeil during the 1970s and 80's demonstrated that the dorsal eyes of Bibionids are functionally adapted to mate detection during high speed female chases for three main reasons.
1) Firstly, male dorsal eyes contain significantly longer rhabdomeres (basic light sensing organelles in the ommatidia of eyes – 2 to 3 times longer in males) than those found in the female eyes or ventral eyes of males.
2) Second, the enlarged retina prominent in male dorsal eyes is characterized by larger facet diameters than those found in male ventral and female eyes, meaning that there is an increase in the aperture area of each facet.
3) Thirdly, Zeil was able to measure interommatidial angles by illuminating fly heads so that light traveled antidromically up the rhabdomeres. This technique revealed that male dorsal eyes have smaller interommatidial angles and different rhabdomere arrangements than ventral or female eyes.
At a functional level, increased aperture area and longer rhabdomere length both serve to increase photon capture efficiency in the male dorsal eye.Zeil, Jochen. 1983. Sexual dimorphism in the visual system of flies: The compound eyes and neural superposition in Bibionidae (Diptera). Journal of Comparative Physiology. 150:379-393. Also, the smaller ommatidial angles and different rhabdomere arrangement observed in dorsal eyes are central to the function of the dorsal eye because they are neural superposition eyes, meaning that neural pooling of information from neighboring ommatidia is used to enhance sensitivity.Zeil, J. 1979. A new kind of neural superposition eye: the compound eye of male Bibionidae. Nature, 278: 249-250. Using a model that takes longer rhabdomeres, larger facet diameters, smaller ommatidial angles, and neural superposition into account, Zeil shows that the dorsal eye of males is able to detect small objects against a homogeneous background at a much greater distance than ventral or female eyes. The optical properties of longer rhabdomeres, increased facet diameter, and smaller ommatidial angles also aid in detection of small objects by increasing the resolution up to six times that of ventral or female eyes when neural pooling resulting from superposition is taken into account. Greater sensitivity to small light changes due to longer rhabdomeres and increased facet diameter, in combination with the ability to detect females at farther distances with higher resolution, allows male Bibionid flies to search for females at lower light levels (greater portion of the day) and to respond quickly to the presence of a female in order to catch her and initiate the "marriage by capture" that occurs in this family of flies. Unlike other fly families, the extreme dimorphism seen in Bibionids may be particularly relevant because these species do not swarm under a landmark, causing the course of females to be relatively unpredictable. As in the olfactory example above, the functional consequences of sex differences in Bibionids are linked to sex-specific behavior for which these sex differences play a key adaptive role.
Auditory system of frogs