HOLLOWS, PEEPERS, AND HIGHLANDERS: AN APPALACHIAN MOUNTAIN ECOLOGY

13. Darter Daddies

89 13 Darter Daddies D arters, as brightly colored as rain forest butterflies and coral reef fishes, are the fish analog to lungless salamanders — both have radiated extensively in the fractured landscape of Appalachia. Darters in the genus Etheostoma draw my attention because of their multifarious forms of parental care. Males alone care for the eggs after the females have deposited them. Some lay their eggs on plants, logs, and other exposed substrates; others form a multi-layered cluster of eggs on the undersides of flat-bottomed rocks; the remainder deposit eggs in a single layer directly on the undersides of flat-bottomed rocks. A fish in the last category, the tessellated darter, has intrigued me for several years, especially after I observed in them an unusual behavior among animals: males caring for eggs that were fertilized by other males. The tessellated darter lives throughout the Atlantic drainages of Appalachia. Male tessellated darters defend flat-bottomed rocks as spawning grounds. When a ripe female approaches a spawning rock, the territorial male flares his fins and quivers his body, then leads her to his rock. Just before she reaches the rock, he scoots under it, inverts belly-up, and begins wiggling across the ceiling. Through this behavior, he seems to be advertising his willingness and ability to clean eggs. In response, she swims under the rock, and inverts and wiggles, probably inspecting the ceiling’s quality. If the male’s courtship is successful, the female begins depositing eggs, one at a time, directly on the bare rock ceiling. As she attaches each egg, the male 90 simultaneously fertilizes it. After the female deposits ten to fifty eggs in a loose two-dimensional cluster, the male chases her away and begins caring for the eggs. If still gravid, the female may approach another nest and mate again. The male scrubs the eggs with his ventral fins while swimming upside down. At the nest’s entrance and while right-side-up, he aerates eggs by maintaining his position with his pectoral fins and pushing water into the nest with his caudal fin. Both cleaning and aerating the eggs burn calories and preclude other activities, such as courting females. Thus, caring for one batch of eggs reduces the total number of eggs a male could potentially fertilize. So far, this scene does not challenge conventional evolutionary ideas. The quirk is that males routinely clean and aerate eggs fertilized by other males. The first time I saw a male cleaning eggs I knew had been fertilized by another male, I could feel Darwin’s grip squeeze my Adam’s apple. It was hard to swallow. Weaned on neo-Darwinian paradigms, I started mumbling to myself on the streambank, alternately feeling excited and confused. The darter’s behavior, if consistently displayed by other males of the population, could be an exciting exception to the dogma that the function of behavior is to promote individual reproductive success. Or it could be a distant outlier explainable by extending the concept of natural selection. During the next three years I dissected the tessellated darter’s social system, carrying out a series of experiments to uncover the causes of this altruism. I studied this darter in a small stream that offered only a few rocks suitable for spawning because most rocks were smothered by heavy silt. The silt blanket and a dense population of darters meant there were more adult males than suitable breeding sites. Consequently, only a few large, dominant, territorial males were able to secure a spawning rock. This left smaller males, which composed the majority, without rocks. Small, subordinate males, or floaters, spent most of their time roaming the stream in search of suitable nest rocks. During his first day of fatherhood, a male scrubs the ceiling, aerates eggs, and repulses potential egg predators. Quite the model Hollows, Peepers, and Highlanders 91 father, he swims only an inch or two from his brood. Mother, long gone, contributes nothing thereafter to embryonic survival. When the embryos reach two days of age, father begins to stray. During extended forays several times per hour, he visits a series of other nest rocks, bullies his way into occupied nests, chases off attendant males, and attempts to usurp fertilizations. Cruising male darters embody the tradeoff between monogamous commitment and promiscuous behavior (a conflict exhibited by some male humans). What opens the door to daddy’s profligate behavior...