Mixed-sex phenotypes in the andean condor: naturally occurring abnormality or environmentally induced disorder?

Sexual dimorphism, i.e., the phenotypic differences between males and females of the same species, is quite common among birds but the only vulture with clearly defined sexual differences is the Andean Condor (Vultur gryphus). There are several sex-specific phenotypic differences between adult males and females in this species, but three important differences are (1) body mass, in which males are up to twice the weight of females, (2) the presence of a comb, which crowns the head of males but is absent in females, and (3) the color of the iris, which is light brown in males and scarlet red in females (Fig. 1A, B). Curiously, in Andean Patagonia in autumn 2018 we observed an individual condor displaying a mixed-sex phenotype (Fig. 1C), somewhat similar to the phenomenon we had previously observed in three condors we trapped for other research on a sheep ranch located 15 km from Bariloche city, Argentina (Fig. 1D). The general phenotypic appearance of these individuals resembled that of female condors, with rudimentary-to-conspicuous combs, possibly as a result of some form of sex reversal. Sex reversal implies some degree of decoupling between an individual’s genetic, gonadal, and phenotypic sexes (Major and Smith 2016). For birds, the sex chromosome constitution established at fertilization dictates the individual’s gonadal identity, whereas the action of steroid sex hormones secreted from the gonads (most notably estrogen and testosterone) then directs phenotypic sexual differentiation (Chue and Smith 2011). Thus, for example, in species showing sexual dichromatism in plumage, the inheritance of female sex chromosomes (i.e., ZW chromosomes) generally results in ovary development and the synthesis and secretion of estrogen are responsible for the subsequent development of female-typical plumage (Owens and Short 1995). Sexually dichromatic plumage coloration is then an estrogen-dependent sex character, meaning that it responds to the presence or lack of estrogen rather than to the presence or lack of testosterone. In the same sense, other characters such as spurs, wattles, and combs are typically testosterone-dependent structures (Owens and Short 1995). In fact, manipulative experiments have shown that both estrogenand testosterone-dependent sex characters can be reverted by altering the levels of the corresponding hormone both during the embryonic life and adulthood (Major and Smith 2016). On this basis, we hypothesize that the unusual appearance of the documented phenotypes can stem from altered sex steroid levels. However, whether they were genotypic females or males remains an open question as the unexpected nature of our observations prevented us from conducting genetic sex determination. Hormonal imbalance can be associated with naturally occurring abnormalities, but also with environmentally induced disorders. Naturally occurring abnormalities include certain congenital neoplasms that affect the gonads and/or adrenal glands and trigger hormonal discord. The occurrence of such disorders has, however, only rarely been reported in poultry and its linkage with cases of sex reversal in wild birds is unclear (Reece 1992, Saif et al. 2008). On the contrary, there is solid and growing evidence that many anthropogenic contaminants are able to alter steroid sex hormone biosynthesis and ultimately affect the development and expression of the maleand female-typical characters (Fry 1995, Mnif et al. 2011). In particular, pesticides are among the most powerful and widespread endocrine-disrupting chemicals, the effects of which have been largely noted in fishes, amphibians, reptiles, birds, and mammals (Guillette et al. 1995). Unfortunately, there exists some evidence that also points to sublethal pesticide poisoning as a likely cause of the presumptive sex-reversed Andean Condors documented here. Andean Condor populations are increasingly exposed to contamination by pesticides. The use of poison-baited carcasses to deliberately kill wildlife is likely one of the most important source of contamination, and Andean Patagonia 1 Email address: pabloalarcon@comahue-conicet.gob.ar