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Mate Choice by Both Sexes Maintains Reproductive Isolation in a Species Flock of Pupfish (Cyprinodon Spp) in the Bahamas Rhiannon J

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Mate Choice by Both Sexes Maintains Reproductive Isolation in a Species Flock of Pupfish (Cyprinodon Spp) in the Bahamas Rhiannon J ethologyinternational journal of behavioural biology Ethology Mate Choice by Both Sexes Maintains Reproductive Isolation in a Species Flock of Pupfish (Cyprinodon spp) in the Bahamas Rhiannon J. D. West & Astrid Kodric-Brown Department of Biology, University of New Mexico, Albuquerque, NM, USA Correspondence Abstract Rhiannon J. D. West, Department of Biology, University of New Mexico, Albuquerque, NM, Female and male mate choices can reinforce reproductive isolation after USA. sympatric speciation. Using a binary choice design, we examine the E-mail: [email protected] importance of visual cues in female mate choice in all three sympatric spe- cies of pupfish on San Salvador Island. We also examine the importance Received: December 2, 2014 of olfactory cues in female choice of the hard-shelled invertebrate special- Initial acceptance: February 2, 2015 ist (Cyprinodon brontotheroides). We examine male mate choice in two of Final acceptance: April 10, 2015 the three species, the scale eater (C. desquamator) and the detritivore (S. Foster) (C. variegatus). Females of all three species use visual cues and prefer con- specific males. C. brontotheroides females do not use olfactory cues to dis- doi: 10.1111/eth.12394 criminate between conspecific and heterospecific males. Males of Keywords: female mate choice, frequency- C. desquamator and C. variegatus also preferentially court conspecific dependent selection, male mate choice, females. Thus, mutual mate choice, where both females and males exhibit olfactory cues, reproductive isolation, mate choice, acts as a strong behavioral pre-mating isolation mechanism sympatric speciation, visual cues in these sympatrically speciated pupfish. (Gazella marica; Wronski et al. 2012), guppies (Poecilia Introduction reticulata), haplochromine cichlids (Astatotilapia flavii- To date, studies of behavioral pre-mating isolating josephi) and swordtails (Xiphophorus malinche) in all of mechanisms in sympatric species flocks have focused which males preferentially court larger, gravid mostly on female choice (Strecker & Kodric-Brown females (Sargent et al. 1986; Dosen & Montgomerie 1999; Kodric-Brown & Strecker 2001; Elmer et al. 2004; Werner & Lotem 2006; Tudor & Morris 2009). 2009; Kahn et al. 2010; Kekal€ ainen€ et al. 2010; Sexual selection can facilitate sympatric speciation Kodric-Brown & West 2014). However, mutual mate (Ritchie 2007), particularly when the divergence is choice, where both sexes preferentially mate with based upon invasion of a new ecological niche (Maan phenotypically similar individuals, would facilitate & Seehausen 2011) and is a signal of localized adapta- sympatric speciation and reinforce species barriers tion (van Doorn et al. 2009). Generally, sexual selec- afterward. Mate choice by females is the classic tion in conjunction with ecological niche expansion paradigm of sexual selection, and thus, the most results in behavioral pre-zygotic isolation that main- investigated mechanism for maintaining behavioral tains species boundaries (Strecker & Kodric-Brown pre-zygotic reproductive isolation. However, selection 2000; Coyne & Orr 2004; Savolainen et al. 2006; imposed by male preferences for mates also shapes Elmer et al. 2011). the evolution of female traits (Andersson 1994). Male Here, we examine male mate choice in Cyprinodon mate choice is common in breeding systems with variegatus and C. desquamator two members of a three paternal care of offspring (Gwynne 1991; Chen et al. species flock of pupfish in the Bahamas. Male mate 2012; Myhre et al. 2012), but a growing literature has choice would reinforce behavioral pre-mating isola- shown that it can occur in the absence of paternal tion in this species flock as has been seen in some sys- care (Edward & Chapman 2011). Examples include tems (Espinedo et al. 2010; Swenton 2011; Gregorio insects (as reviewed in Bonduriansky 2001), gazelles et al. 2012), but not others (Kozak et al. 2009). Ethology 121 (2015) 793–800 © 2015 Blackwell Verlag GmbH 793 Mate Choice Maintains Reproductive Isolation R. J. D. West & A. Kodric-Brown We also examine the role of both visual and olfac- and reddish orange fins and belly in C. variegatus, and tory cues in female mate choice in C. desquamator and a pale blue body with clear pectoral fins outlined with C. brontotheroides. Both kinds of cues function in mate black in C. brontotheroides (Martin & Wainwright choice in other pupfish (Kodric-Brown 1983, 1996; 2013a; personal observation). However, as in most Strecker & Kodric-Brown 1999, 2000; Kodric-Brown pupfish studied to date, male breeding coloration is & Stecker 2001; Ludlow et al. 2001; Draud & Itzko- facultative and can be turned on or off almost instan- witz 2004) and play a role in promoting or maintain- taneously (Kodric-Brown 1998; Barton & Barton ing reproductive isolation in a variety of other kinds 2008). Territories provide incidental protection of eggs of organisms (Elmer et al. 2009; Smadja & Butlin from predation, as males chase away females who are 2009; Hohenlohe & Arnold 2010). We focused on attempting to forage on the territory. Territories of female preferences in the scale eater C. desquamator C. desquamator are smaller than those of C. variegatus, and the hard-shelled specialist C. brontotheroides.To are usually located in shallower water, and are con- date, little is known about female preferences in the fined to small, rocky outcrops near the shoreline. scale eater in either the field or the laboratory (Barton Male C. variegatus courtship consists of circling below & Barton 2008; Kodric-Brown & West 2014), and a female and guiding her toward the substrate, while nothing about female preferences in the hard-shelled C. desquamator males approach the female in a series invertebrate specialist. We focused on mate choice of rapid zigzag or darting movements and lead her to because it will not only provide information on the the territory. In sequential trails, male detritivores proximal mechanisms, such as the sensory cues used court female conspecifics and scale eaters equally, in courtship and mating in each species, but it also whereas male scale eaters preferentially court conspe- will provide insights into the evolution of pre-mating cifics (Kodric-Brown & West 2014). Territorial males isolation in a very young species flock. rarely shoal with conspecific females and juveniles. Generally, territorial male detritivores and scale eaters The System only shoal when they are disturbed, for example, by a predator or an ungainly biologist, and quickly return Three sympatric species of pupfish occupy three saline to their territories (personal observation). C. brontot- lakes on San Salvador Island, The Bahamas (Holtme- heroides are very scarce in all three lakes and much of ier 2001; Turner et al. 2008; Martin & Wainwright their behavior is unknown. 2011). The species evolved in the last 6000 yrs, when the lakes formed on the island (Pacheco & Foradas M&M 1986; Hagey & Mylroie 1995; Milliken et al. 2008). The species flock consists of a relatively rare scale Female Mate Choice eater, C. desquamator which preys upon the other two species, a very abundant detritivore, C. variegatus, and We examined the strength of female preferences for a very rare hard-shelled prey specialist, C. brontothero- conspecific males in F1 populations of C. variegatus, ides (Holtmeier 2001; Turner et al. 2008; Martin & C. desquamator, and C. brontotheroides from Crescent Wainwright 2013a). The species differ in morphology, Lake. It is one of the smallest lakes on San Salvador ecology and behavior related to trophic specialization Island with populations of all three species of pupfish (Holtmeier 2001; Barton & Barton 2008; Turner et al. and has the highest densities of C. desquamator. Labo- 2008; Martin & Wainwright 2011, 2013a; Kodric- ratory raised offspring from wild-caught parents were Brown & West 2014; West and Reade in prep). Species used to lessen potential trapping impacts on all three isolation is likely maintained by behavioral pre-zygotic species, but especially on the rare C. brontotheroides. isolation as the three species coexist in sympatry with The parental populations consisted of 15 C. brontother- overlapping habitats but readily hybridize in the labo- oides and 20–30 individuals each of C. variegatus and ratory (Holtmeier 2001). In the field, there are large C. desquamator. The parental fish were housed by spe- fitness costs to hybrids (Martin & Wainwright 2013b). cies and bred in large (1.89 kl) stock tanks with a C. variegatus and C. desquamator have a polygynous 14:10 light:dark schedule and salinity at 35 ppt., con- mating system with males defending contiguous terri- sistent with salinities in Crescent Lake. Under natural tories. Females mate with multiple males and deposit conditions in the lake, fish are exposed to heterospe- several eggs on a male’s territory during a spawning cifics and therefore avoidance may be learned. We sequence. Males defending territories develop breed- raised the fish in separate tanks for several reasons: (i) ing coloration that varies from black on the body and all three species readily hybridize in captivity; (ii) our fins in C. desquamator to blue iridescent on the nape design removes the role of learning and experience of 794 Ethology 121 (2015) 793–800 © 2015 Blackwell Verlag GmbH R. J. D. West & A. Kodric-Brown Mate Choice Maintains Reproductive Isolation heterospecifics from potentially influencing mate The males were then replaced with a novel combina- choice, and (iii) prevents harassment and excessive tion of males
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