The Evolution of Derived Monomorphism From Sexual Dimorphism: A Case Study on Salamanders

Sexual dimorphism, differences between males and females in secondary sexual characteristics, has long interested biologists in part because it is unexpected. Perhaps, because of this, sexual dimorphism has been widely studied (e.g., Ralls 1977; Slatkin 1984; Stamps 1993; Fairbairn 1997; Butler et al. 2007; Cox and Calsbeek 2009; Stewart and Rice 2018; Houle and Cheng 2020). Sexual dimorphism is not expected, or should be slow to evolve on theoretical grounds, because of the genetic correlation between sexes (Lande 1980), at least over short time scales (McGlothlin et al. 2019). While the genetic correlation between males and females can restrict the extent of dimorphism (Poissant et al. 2010), the historical focus on sexual selection on males contributed to the perspective that many female secondary sexual characteristics (traits developing at sexual maturity) that were similar to those in males, were merely a consequence of this genetic correlation and not a result of selection on the female in her own specific social context (Amundsen 2000). Researchers have argued that the evolution of the female phenotype can be better explained by independent selection on females (e.g., Ralls 1976; Burns 1998; Amundsen 2000; Clutton-Brock 2007, 2009). Furthermore, identifying the selective forces underlying sexual dimorphism illustrates that differential selection on both sexes determines the extent of sexual dimorphism (blackbirds: Irwin 1994; tanagers: Burns 1998; house finches: Badyaev and Hill 2000; Drosophila: Chenoweth et al. 2008). In comparison to sexual dimorphism, monomorphism has received less attention because it is predicted from simple theoretical expectations. Monomorphism is assumed to be the ancestral state for most groups and hence seems less interesting; there is no obvious signature of selection differentiating the sexes. Sexual monomorphism, however, can be a derived condition, evolving from sexual dimorphism. Derived monomorphism is the condition in which both males and females express the same derived features and thus are monomorphic, but differ from an ancestrally monomorphic condition as well as from the sexually dimorphic intermediate. Darwin (1871) was the first to identify this pattern of derived monomorphism and called it transference. He observed that females of some bird species possessed bright coloration and elaborate plumage and consequently closely resembled males, whereas in other species, females appeared drab and plain-colored. He proposed that from color dimorphism, color monomorphism was achieved through the transference of male characteristics to the female. In regard to the differences between the females within the same genus, it appears to me almost certain, after looking through various large groups, that the chief agent has been the greater or less transference to the female of the characters acquired by the males… (Darwin 1871, 793). West-Eberhard (2003) argued that derived monomorphism, or cross-sexual transfer as she called it, is an important cause of evolutionary novelty via social selection. I examine the patterns of sexual dimorphism and monomorphism in the salamander genus Aneides (family Plethodontidae). Social selection occurs in the context of interactions among conspecifics and is defined as “differential reproductive success… due to differential success in social competition, whatever the resource at stake” (West-Eberhard 1983, 158). Social selection predicts sexual dimorphism if the involvement of females and males in relevant social interactions is unequal and predicts the evolution of derived monomorphism from dimorphism when both sexes are involved nearly equally (West-Eberhard 1983). Sexual selection then is a type of social selection that typically results in sexual dimorphism. Ecological causes of sexual dimorphism that involved social interactions at some point in their evolution, such as competitive displacement (Slatkin 1984; Hedrick and Temeles 1989; Shine 1989), are also included within social selection. Derived monomorphism, and the social context of its evolution, has been studied in varied taxa. For example, social competition is argued to result in exaggerated yet monomorphic coloration in lek-breeding birds (Trail 1990) and hummingbirds (Bleiweiss 1985). In hyenas (Crocuta crocuta), females express androgenized traits compared to other carnivores, including external genitalia, increased body size and weight, and aggressive behavior (Matthews 1939; Dloniak et al. 2006; Hammond et al. 2012). Derived monomorphism has also been reported in ungulates (Kiltie 1985; Geist and Bayer 1988) and butterflies (Vane-Wright 1980, 1984; Clarke et al. 1985; Cook et al. 1994). Plants also show derived monomorphism (primroses: Mast et al. 2006). One of the earliest uses, perhaps the first, of the term derived monomorphism is in a description of derived monomorphic pollen (Baker 1948). This too was set in a social context of the evolution of self-incompatibility and a potential adaptation to sparse pollinators (Baker 1948). Derived monomorphic females are often referred to as being “masculinized” or expressing “male-typical” traits. These terms are problematic, however, as these traits are typical female traits in these species with derived monomorphism. A more appropriate term for these traits is simply “derived monomorphic,” which refers to traits in one sex (male or female) that were ancestrally limited in expression to the other sex (male or female). One can imagine it would be useful to retain the information of which sex evolved the trait initially, in which case the longer term “male-to-female derived monomorphism” could be used, for example. Fanged frogs (Limnonectes blythii) of Southeast Asia show some female-to-male derived monomorphic traits such as low androgen levels, lack of nuptial pads, and parental care (Emerson et al. 1997). Another potential case of derived monomorphism is if one sex loses its derived sexually dimorphic trait over time and the resulting monomorphic state is thus derived. I focus on the case, however, in which one sex evolves the expression of a derived trait that is ancestrally limited in expression in the other sex. Sexual dimorphism in plethodontids Sexual size dimorphism is common in salamanders of the family Plethodontidae but typically is not profound, with females slightly larger than males (Shine 1979; Bruce 2000; Kupfer 2007). In amphibians, female body size is correlated with egg number, and thus female-biased size dimorphism is thought to primarily result from fecundity selection (Salthe and Duellman 1973; Shine 1979), although other factors may be important as well (Shine 1988). In a review of sexual size dimorphism among families of amphibians, selection on female body size was found to be the driver behind most sexual dimorphism (De Lisle and Rowe 2013). Important exceptions to this general pattern include the plethodontid genera Phaeognathus and Desmognathus, which have male-biased sexual dimorphism in body length (Bruce 1993, 2000; Bakkegard and Guyer 2004; Camp et al. 2019). Because Desmognathus and Phaeognathus are sister-taxa to Aneides (Fig. 1), but more distant relatives (e.g., Plethodon, Karsenia) are monomorphic, male-biased size dimorphism appears to be ancestral for Aneides. Analyses based on sequences of 50 nuclear markers find that Aneides diverged from a common ancestor with Desmognathus about 38–45 mya (Shen et al. 2016). The genus Aneides is characterized by (among other features) a single, rather than a paired, premaxillary bone (shared with the desmognathans among plethodontines) and by a rearrangement of the carpal and tarsal mesopodial elements (Wake 1963, 1966), the latter unique to Aneides among plethodontines. These 2 features, considered as key innovations, form the basis of a suite of morphological and ecological features associated with strengthening the skull and grasping ability (Wake 1963, 1966; Larson et al. 1981). In addition, the species of Aneides examined thus far exhibit dimorphism in the degree of jaw muscle hypertrophy and in features of the skull, including dentition (Wake 1963; Lynch 1981; Staub 2016). Open in a separate window Fig. 1 (a) Phylogeny of Aneides. There are 3 distinct species groups: the lugubris group, the hardii group, and the aeneus group (Wake, 1963). Tree is adapted from Vieites et al. (2007), Shen et al. (2016), Patton et al. (2019), Reilly and Wake (2019), and Jackman (1998); branch lengths are not representative of evolutionary change or time. (B) Phylogeny showing one hypothesis for the evolution of derived monomorphism in Aneides. Sexual dimorphism in body length, with males being longer than females, is ancestral for Aneides. HW dimorphism is a synapomorphy of Aneides, with male heads wider than females. Derived monomorphism has evolved in the aeneus and lugubris species groups, with females expressing derived monomorphic traits of jaw muscle hypertrophy and larger size. Female A. lugubris show a derived increase in SVL. (C) For this hypothesis of the evolution of derived monomorphism in Aneides, derived monomorphism is a synapomorphy of the genus (males and females do not differ in body length or HW) and subsequently female A. hardii lost the derived monomorphic traits in HW and SVL, and female A. lugubris increased in SVL. In the cartoon diagrams, the female is above the male in each pair.