Evolution of Primary Sexual Characters in Amphibians

In the fi rst modern text dedicated to the biology of the Amphibia, Noble (1931) devoted an entire chapter to secondary sexual characters. We focus briefl y on these secondary characters to distinguish them from our main consideration, the primary reproductive traits. Noble defi ned secondary traits operationally (p. 108) as “all the differences between the two sexes other than those connected with the gonads and their ducts” (note that Noble makes no mention of either natural or sexual selection). As might be expected for the Anura, Noble devotes a good deal of space to discussing sexually dimorphic traits, such as nuptial pads on thumbs, enlarged larynxes, and vocal sacs of various kinds. For both the Anura and Urodeles, Noble also mentions certain kinds of skin glands that are related to reproduction. For anurans, we now believe these glands are used in mate attraction and, in a sense, are the chemical equivalents of mating calls (e.g., Wabnitz et al. 1999; Pearl et al. 2000; see also Brizzi et al. 2002). In salamanders, specialized skin glands are related to identifi cation of species and sex (Dawley 1984, 1986), and also to infl uencing female receptivity to a courting male (Houck & Reagan 1990; Houck et al. 1998; Rollmann et al. 1999). These specialized traits all have been promoted by sexual selection. In contrast to the specializations above, Noble (1931) considered that, for all amphibians, only differences between the sexes that related to the gonads and their ducts would be classifi ed as primary sexual characters. To quote Darwin (1871, pp. 253, 254), “Unless indeed we confi ne the term ‘primary’ to the reproductive glands, it is scarcely possible to decide which [reproductive traits] ought to be called primary and which secondary” (also see Grant 1995 for similar comments on plants). Here, following both Darwin and Noble, we restrict our discussion of amphibians primarily to gametes, gonads, oviducts, and associated structures required for ova and sperm to unite. As natural selection also acts on other reproductive traits, however, we also include observations of evolutionary change in basic reproductive characteristics. In particular, we consider mating behaviors associated with sperm transfer, physiological cycles (e.g., annual changes in levels of androgen), and female retention of fertilized ova until larvae (or metamorphosed young) are released. We consider these additional reproductive traits to be governed by natural selection (e.g., survivorship of offspring) rather than sexual selection. Also, in contrast to expectations for sexually selected traits, we expect relatively less variation among conspecifi c males or females in primary characters shaped by natural selection (although trait expression may vary with age or body size). Presumably, these primary traits are under strong stabilizing selection, as mentioned below for the “tail-straddling walk” that has characterized the mating behavior of plethodontid salamanders for over 15 million years. In many areas, much more information has been published on anurans and salamanders than is available for the third group of amphibians, caecilians.