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Notes and Comments

This note suggestsa connection between a finding in molecular genetics, the molecular evolution of a-lactalbumin from lysozyme, and a problem that has been debated by evolutionary biologists for over a century, the evolution of milk production. All of the hypotheses for the evolution of lactation (reviewed by Long, 1969, 1972; Graves and Duvall, 1983) implicitly or explicitly rely on the following scenario, as expanded from that of Darwin (1872): 1) increased proximity of mother and newly laid eggs, perhaps with the maternal development of a vascularized, abdominal, incubation patch; 2) enhancement of offspring (eggor hatching) survivorship through secretionby maternal cutaneous glands; 3) accidental ingestion or absorption of maternal secretions by offspring and their subsequent use as food or drink; 4) concomitant development ofsuckling behavior, localized areolar regions, and an increased nutritional value ofthe maternal secretions. Although they are not mutually exclusive, the available hypotheses differ with respect to the primary adaptive benefit ascribed to the hypothetical protolacteal secretions. The presumed advantages currently fall into three classes: 1) thermoregulation of eggs or young via evaporative cooling (Haldane, 1965) or heat transfer from the mother (Bresslau, 1907; Gregory, 1910); 2) maintenance of water balance of the eggs or hatchlings, e.g., prevention of desiccation (Haldane, 1965); 3) maintenance of proximity of the mother and her offspring (egg or young) either mechanically via albuminous glue (Gregory, 1910), or behaviorally via aggregation pheromones simultaneously operating as milk precursors (Graves and Duvall, 1983). As an addition to this list we propose a hypothesis that ties the molecular evolution of a major component of the milk synthesis system to the functional modifications accompanying the evolution oflactation from preexistingsystems. These systems may have served very different roles in the lives ofthe earliest mammals and their ancestors. We hypothesize that protolacteal secretions helped protect the eggsor young from bacterial, protozoal, or fungal infection. The genesis of this hypothesis lies in the already documented (Brew et al., 1967, 1970; Smith, 1970; Gordon, 1971; Dayhoff, 1976) evolution of a gene for a-lactalbumin from a duplication of the genetic material for lysozyme. a-lactalbumin has been found only in therian mammals and is a subunit of the lactose synthetase system within the mammary gland (Brew, 1969; Jones, 1977). Lysozyme is a bactericidal and fungicidal enzyme (Tizard, 1981; Marquis et al., 1982) which is found in all major groups of organisms (Dayhoff, 1976)and is also present in mammalian milk (Hopper and McKenzie, 1974). a-lactalbumin has not been found in the egg-layingmammals, the platypus and the echidna. However, echidna milk possesses a lysozyme that not only has the antibacterial and structural properties, but also has activity in the lactose synthetase system (Hopper and McKenzie, 1974). Thus, monotremes appear to have a protein which is a structural and functional intermediate between that of lysozyme and a-lactalbumin. Following Dickerson and Geis (1969), and Gould and Vrba (1982), we envision the duplication of the genetic material for lysozymes occurring perhaps as early as 300 million years ago (Dayhoff, 1976).Subsequently, the duplicated material evolved, and its product was used in the milk-producing system perhaps via an intermediate form that possessed both functions as does the lysozyme in echidna milk. This suggests that although the gene for lysozyme may have duplicated much earlier, the evolution of a-lactalbumin did not occur until after the prototherian/therian split. The probable evolution of a-lactalbumin from lysozyme implies that lysozyme was secreted by the mammary gland precursors, just as it is currently secreted by certain other glands of ectodermal origin (e.g., lacrimal glands, Sapse et al., 1968; salivary glands, Miyauchi, 1984). The precursors to other milk proteins with anti-microbial properties, i.e., lactoferrin and lactoperoxidase (Morrison and Allen, 1966; Arnold et al., 1977), may also have been present. We suggest that the protolacteal secretion enhanced the survival of the eggs or young by virtue of its anti-microbial properties. The microbial environment surrounding the eggs is probably im-