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One of the defining characteristics of Elasmobranchii is the external gill slits, through which water is expelled during exhalation. The morphology of the gill slits is presumed to vary among elasmobranchs, between ram and suction ventilators, and between pelagic and benthic species. However, the evolution of gill slit morphology and the relationship to behavior and ecology is not clear. The relative length of each slit, relative distance between adjacent pairs of slits, and number of slits positioned over the pectoral fin were quantified in 289 preserved specimens representing 185 species in 69 genera, 28 families, and 8 orders of sharks. Six character states of relative gill slit length, five character states of relative inter-gill slit spacing, and five gill slit positions over the pectoral fin were identified. Character mapping onto a phylogeny reveals that the basal state for extant Selachii is to possess slits of similar relative length and spacing with no slits over the pectoral fin. Multiple character states in various combinations evolved within the Carcharhiniformes, which is the most speciose extant group. Ontogenetic differences in gill slit morphology were found in the 12 genera in which adult and juvenile data were collected. Slit spacing in juveniles has an equal tendency to become more similar or more different in adults, whereas slit length changes more often from more similar in juveniles to increasingly different in adults. Exploring the relationships among gill slit morphology and ventilation mode in modern sharks reveals character complexes that are common to four body types. Macropelagic types are ram ventilators with a longer first slit length, similar slit spacing in most, and no slits over the pectoral fin. Most littoral types are ram ventilators, with decreasing slit length and spacing and with one slit over the fin. Benthic types are suction ventilators with decreasing slit length and spacing and up to four slits over the fin. Bathic and micropelagic types are suction ventilators with no slits over the fin and most having similar slit length and spacing. Morphological differences in gill slit morphology may correspond to hydrodynamic differences in exhaled water from the slits by habitat.