Do Female Western Mosquitofish, Gambusia Affinis, Prefer Ornaments That Males Lack? Scott L

Montclair State University Montclair State University Digital Commons Department of Biology Faculty Scholarship and Department of Biology Creative Works Fall 2016 Do Female Western Mosquitofish, Gambusia affinis, Prefer Ornaments That Males Lack? Scott L. Kight Montclair State University, [email protected] Olga Degtyareva Heather Fackelman Ariel Casner Follow this and additional works at: https://digitalcommons.montclair.edu/biology-facpubs Part of the Behavior and Ethology Commons, Evolution Commons, and the Zoology Commons MSU Digital Commons Citation Casner, Ariel M., Heather C. Fackelman, Olga Degtyareva, and Scott L. Kight. "Do Female Western Mosquitofish, Gambusia affinis, Prefer Ornaments That Males Lack?." Ethology 122, no. 7 (2016): 561-570. Published Citation Casner, Ariel M., Heather C. Fackelman, Olga Degtyareva, and Scott L. Kight. "Do Female Western Mosquitofish, Gambusia affinis, Prefer Ornaments That Males Lack?." Ethology 122, no. 7 (2016): 561-570. This Article is brought to you for free and open access by the Department of Biology at Montclair State University Digital Commons. It has been accepted for inclusion in Department of Biology Faculty Scholarship and Creative Works by an authorized administrator of Montclair State University Digital Commons. For more information, please contact [email protected]. Ethology RESEARCH PAPER Do Female Western Mosquitofish, Gambusia affinis, Prefer Ornaments That Males Lack? Ariel M. Casner, Heather C. Fackelman, Olga Degtyareva & Scott L. Kight Department of Biology, Montclair State University, Montclair, NJ, USA Correspondence Abstract Scott L. Kight, Department of Biology, Montclair State University, Montclair, NJ Some species in the family Poeciliidae are known for extravagant male 07043, USA. ornaments and courtship behavior (e.g., guppies), but the majority of poe- E-mail: [email protected] ciliids are characterized by coercive male copulation attempts that seem to circumvent female choice. In some lineages with male ornaments, female Received: March 31, 2016 sensory bias may have preceded the evolution of corresponding male sig- Initial acceptance: April 11, 2016 nals. We examined female preferences for colorful ornaments in Western Final acceptance: April 11, 2016 mosquitofish, Gambusia affinis, in which males lack ornamentation and (E. Hebets) reproduce primarily through coercive mating attempts. We found that females exhibited a positional affinity for males that were artificially orna- doi: 10.1111/eth.12507 mented with blue coloration over males that had been treated with a Keywords: Gambusia affinis, mate choice, transparent ornament. Females exhibited the opposite effect for males sensory exploitation, Western Mosquitofish treated with red ornaments. In contrast, focal females did not exhibit behavioral discrimination between two live stimulus females or two mod- els (silver fishing lures) with blue vs. transparent ornaments. This suggests a sexual context for female discrimination between males based on ornament color and whether an ornament was present. Because tribe Gambusiini is the basal branch of family Poeciliidae, the results of this study are consistent with the hypothesis that female responsiveness to male coloration is the ancestral poeciliid character state. species of the poeciliid genus Xiphophorus evolved in Introduction concert with a preexisting female bias for this shape. The evolutionary tug-of-war between traits that In swordless congeners (platyfish), females prefer increase survivorship and those associated with sexual males with experimentally affixed prosthetic swords. attraction has been the subject of much attention Some phylogenetic analyses of the genus suggest that since Charles Darwin introduced his theory of sexual the female preference for swords evolutionarily pre- selection (Darwin 1871; Fisher 1930; Hamilton & Zuk ceded the appearance of the male signal (Rosen 1979; 1982; Parker 2006). Many animal species, from pea- Rauchenberger et al. 1990; Basolo 1990, 1991; but fowl (Petrie 1994) to sticklebacks (Rowland 1994), see Meyer et al. 1994). Indeed, the preference for exhibit costly male behavior and ornaments that are swords extends into other related, but swordless, gen- associated with corresponding female mating prefer- era (Basolo 1995). ences. The interaction between sexual selection and Given this sensory exploitation hypothesis (see other forms of natural selection is therefore particu- Ryan 1990) that preexisting sensory biases in females larly interesting when females exhibit mating prefer- drove the evolution of male secondary sexual charac- ences for characteristics that males do not have. ters in Xiphophorus, we were curious about the rela- A mismatch between female preference and male tive lack of male ornamentation in other poeciliid signal is apparent when congeneric females have sim- lineages. Beyond Xiphophorus and Poecilia (guppies), ilar mating preferences, but males of some species lack male sexual ornaments are relatively rare in the the corresponding signal. For example, Basolo (1995) family Poeciliidae, where lack of male courtship and proposed that the sword-shaped male tail in some ornaments appears to be the ancestral state (Bisazza Ethology 122 (2016) 1–10 © 2016 Blackwell Verlag GmbH 1 Ornament Preferences in Female G. affinis A. M. Casner, H. C. Fackelman, O. Degtyareva & S. L. Kight et al. 1997). Whether female preferences for male males, and the mismatch between female association ornaments are ancestral or derived within the Poecili- with larger males but high copulatory efficiency of idae, however, is currently unknown. If female orna- smaller males suggest that male sexual behavior can ment preference is the ancestral state, we might negatively influence female reproductive success. For expect it to appear in mosquitofish (Gambusia sp.) as example, female mosquitofish spend inordinate tribe Gambusiini appears to be the basal branch of amounts of time avoiding or fleeing coercive males subfamily Poeciliinae (Bisazza et al. 1997). (Pilastro et al. 1997), which can lessen female forag- Mosquitofish are widespread and abundant live- ing efficiency by half (Pilastro et al. 2003) and pre- bearing poeciliids, found on almost all continents sumably reduce the number and size of eggs (Krumholz 1948; Lloyd & Tomasov 1985; Lloyd 1986; produced. Heinen et al. (2013) found that male G. Pyke 2005). The sexes are dimorphic in shape and hubbsi in populations with predators chased females size, with females larger than males and lacking the more frequently. Predators appear to drive selection modified anal fin (gonopodium) that serves as an that favors mating early and often. Female G. holbrooki intromittent organ. However, mosquitofish males typ- mitigate male harassment and improve foraging effi- ically differ little from females in coloration [a notable ciency by shoaling with groups of conspecific females exception is the Bahamas mosquitofish, Gambusia (Bisazza et al. 2001; Pilastro et al. 2003). hubbsi, in which males exhibit orange dorsal col- Sexual selection appears to operate differently oration (Martin et al. 2014; Heinen-Kay et al. 2015)]. among poeciliid lineages, with intersexual selection It is hypothesized and supported that intersexual stronger in guppies (Poecilia) and swordtails selection for male ornaments is driven by female (Xiphophorus), but intrasexual selection generally pre- choice in multiple poeciliid lineages (e.g., guppies: vailing in mosquitofish (Gambusia, but see Heinen- Endler 1983; Houde 1997; swordtails: Basolo 1990). Kay et al. (2015) for a recent study of sexually dimor- Therefore, it seems possible that female preferences phic G. hubbsi). This diversity of mating systems evolved before the basal Gambusiini diverged from among the Poeciliidae suggests that female prefer- other poeciliine tribes. We predict that female mos- ences might be more widely distributed among taxa quitofish may exhibit preferences for ornaments even than corresponding male signals. Bisazza et al. (1997) in species with no corresponding male signals. conducted a phylogenetic analysis of the Poeciliidae Males of most mosquitofish species do not appear to using sequence data from the large (16S) mitochon- use colorful or elaborate traits to attract females. drial ribosomal gene and reached two interesting con- Instead, males are coercive and seem largely devoted clusions. First, the Tribe Gambusiini appears to be the to sexual pursuit and harassment of females with basal branch in the clade, so lack of male ornamenta- attempts at insemination through gonopodial ‘thrusts’ tion is probably the ancestral character state. Second, at female urogenital openings (Haynes 1993; Pilastro male ornaments and courtship behavior likely et al. 1997). Coercive copulation strategies may have evolved independently in Poecilia and Xiphophorus. evolved intrasexually under sperm competition, as If ancestral poeciliid males lacked sexual orna- females store sperm and each brood can have multiple ments, a preference for ornaments by contemporary sires (Constantz 1984). Male mosquitofish with larger female Gambusia would be consistent with a sensory bodies are known to chase and preclude smaller males exploitation hypothesis that preexisting female biases from proximity to females (Itzkowitz 1971; Bisazza drove the evolution of male ornamentation in some and Marin 1995), and there is evidence that females poeciliid lineages. There is some evidence that female prefer to mate, or at least associate with, larger males mosquitofish

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