Sensory drive predicts that the conditions under which signaling takes place have large effects on signals, sensory systems, and behavior. The coupling of an ecological genetics approach with sen- sory drive has been fruitful. An ecological genetics approach compares populations that experi- ence different environments and asks whether population differences are adaptive and are the result of genetic and/or environmental variation. The multi-faceted effects of signaling environ- ments are well-exempliﬁed by the blueﬁn killiﬁsh. In this system, males with blue anal ﬁns are abundant in tannin-stained swamps that lack UV/blue light but are absent in clear springs where UV/blue light is abundant. Past work indicates that lighting environments shape genetic and envir- onmental variation in color patterns, visual systems, and behavior. Less is known about the select- ive forces creating the across population correlations between UV/blue light and the abundance of blue males. Here, we present three new experiments that investigate the roles of lighting environ- ments on male competition, female mate choice, and predation. We found strong effects of lighting environments on male competition where blue males were more likely to emerge as dominant in tea-stained water than in clear water. Our preliminary study on predation indicated that blue males may be less susceptible to predation in tea-stained water than in clear water. However, there was little evidence for female preferences favoring blue males. The resulting pattern is one where the effects of lighting environments on genetic variation and phenotypic plasticity match the direction of selection and favor the expression of blue males in swamps. Key words: Lucania goodei, adaptive plasticity, intrasexual selection, male competition, private communication, predation Twenty-five years ago, John Endler published his seminal paper on 1988) to an ecological and evolutionary audience. Endler particular- sensory drive in the American Naturalist (Endler 1992). In that ly emphasized the role of the environmental conditions on signaling paper, Endler introduced concepts developed in the field of sensory dynamics. Applied to a sexual selection context, sensory drive states ecology (Duntley 1951; Mertens 1970; Lythgoe 1979; Lythgoe the following: Males have traits that they use as signals to obtain V C The Author(s) (2018). Published by Oxford University Press. 499 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact email@example.com Downloaded from https://academic.oup.com/cz/article-abstract/64/4/499/5025950 by Ed 'DeepDyve' Gillespie user on 22 August 2018 500 Current Zoology, 2018, Vol. 64, No. 4 mates. These signals are displayed at various times and places and associated with the outcome of male competition (Andersson 1994; then must travel through the environment and be detected by the Santos et al. 2011; Crothers and Cummings 2015; Johnson and sensory system of the receiver. These sensory properties have strong Fuller 2015; Zhou and Fuller 2016). However, the role of natural influences on a number of behaviors including (a) non-mating traits variation in lighting environments on the outcome of male/male such as the ability to find food, find proper habitat, avoid predators, competition has received little attention. Tinghitella et al. (2015) re- etc. and (b) mating behaviors such as female mate choice and male/ cently tested whether three-spined stickleback males with red throat male competition. Mating behaviors create sexual selection favoring color had a competitive advantage over males lacking red throat certain male traits over others. The evolution of particularly con- color in full spectrum versus red-shifted light (where red throats are spicuous male traits also has the potential to increase male suscepti- absent), but found no effect of lighting environment. Several studies bility to predation. Since its publication, sensory drive has been cited have manipulated lighting environments to disrupt male/male signal- over 1,300 times and in varying ways, ranging from mechanistic ing by eliminating the ability of animals to use specific wavelengths studies of signal generation and sensory system properties (Stieb and color contrasts (Evans and Norris 1996; Baube 1997; et al. 2016; Escobar-Camacho et al. 2017; Phillips and Derryberry Braun et al. 2014; Zhou and Fuller 2015), but few have mimicked 2017) to comparative studies of signal and sensory system properties natural variation in lighting environments to assess its likely effects across broad phylogenetic distances (Ryan and Keddy-Hector 1992; on male competition in the wild. The pattern that emerges is one Gomez and Thery 2007; Stuart-Fox et al. 2007; Ord et al. 2015; De where the direction of selection due to predation, male competition, Lanuza and Font 2016; Gawryszewski et al. 2017; Buchinger et al. and to a far lesser extent, female mate choice coincides with the pat- 2017; Strauss et al. 2017; Stanger-Hall et al. 2018). terns of phenotypic plasticity and genetic variation that favor the The application of an ecological genetics approach to questions presence of killifish with blue anal fins in swamps. surrounding sensory drive has been fruitful (Marchetti 1993; Endler Male color patterns are extremely variable within and among and Houde 1995; Endler 1995; Houde 1997; Boughman 2001; Leal populations of bluefin killifish, Lucania goodei (Foster 1967; and Fleishman 2002; Seehausen et al. 2008; Servedio and Arndt 1971; Fuller 2002). Figure 1 illustrates the variation in male Boughman 2017). An ecological genetics approach relies on identi- coloration. The other intriguing aspect of this system is that bluefin fying traits that co-vary with environmental variables across popula- killifish populations are found in a variety of lighting habitats tions or closely related species and asking (a) whether the including crystal clear springs and tannin-stained swamps correlation between trait values and environment are driven by nat- (Figure 2). Here, we focus on the patterns in male anal fin color- ural and/or sexual selection and (b) whether trait variation is due to ation, which, at first glance, present a paradox: blue males are abun- genetic and/or environmental effects (Travis and Reznick 1998; dant in tannin-stained swamps that have low abundance of UV/blue Reznick and Travis 2001). The merger of sensory drive and eco- wavelengths and where males and females are less sensitive to those logical genetics highlights the multi-faceted effects of environmental wavelengths of light. Figure 2A shows the relationship between the variation. Variation in environmental signaling conditions can result abundance of males with blue anal fins and the relative transmission in genetic differentiation among populations and closely related of UV/blue wavelengths across 30 populations in Florida. Blue males species (Lythgoe et al. 1994; Cronin et al. 1996; Endler et al. 2001; are common in swamp populations that have low transmission of Seehausen et al. 2008; Knott et al. 2017; Nandamuri et al. 2017); it UV/blue wavelengths, and are rare or absent in springs with high can alter the development of signals, sensory systems, and associated transmission of UV/blue (Fuller 2002). Figure 2B shows samples of behaviors (Kroger and Fernald 1994; Cronin and Caldwell 2002; swamp and spring water in white buckets. Figure 2C shows the Fuller and Travis 2004; Hofmann and Carleton, 2009; Knott et al. relative down-welling irradiance spectrum in a spring and a swamp 2010; Ziegler et al. 2011; Ehlman et al. 2015; Sandkam et al. 2016; population (see Supplementary materials and Supplementary Wright et al. 2017; Wright et al. 2018); and it can alter the immedi- Figure 1 for details and absolute irradiance). The visual systems also ate perception of signals by altering their transmission and the back- vary between springs and swamps (Fuller et al. 2003, 2004). Bluefin grounds on which they are perceived (Long and Houde 1989; killifish possess five broad classes of cones: UV, violet, blue, yellow, Seehausen and Van Alphen 1998; Maan et al. 2006; Reichert and and red. Spring animals have a higher relative frequency of UV and Ronacher 2015). Differences in lighting environments can even alter violet cone cells, whereas swamp animals have a higher relative fre- survival in the absence of predation (Maan et al. 2017). Hence, sig- quency of yellow and red cone cells (Figure 2B). The pattern of opsin naling environments can affect among population genetic variation, expression reflects this variation in cone cell types with higher pro- phenotypic plasticity, and the direction of selection. portional expression of the SWS1 and SWS2B (the opsins involved These multi-faceted effects are well-exemplified by the variation in UV and violet cone cells) in springs and high proportional expres- in color patterns, color vision, and visually based behaviors present sion of RH2-1 and LWS (the opsins involved in yellow and red cone in the bluefin killfish Lucania goodei. In this article, we first review cells) in swamps (Figure 2C). Electroretinogram studies also indicate the previously published literature on (a) the among population cor- that swamp animals are less sensitive to UV/blue light than spring relations between color patterns, visual systems, and signaling envi- animals (Fuller et al. 2003). These population patterns present ronments and (b) the multi-faceted effects of lighting environment somewhat of a paradox, because blue males are common in habitats on the phenotypic expression of male coloration, visual system that lack UV/blue light and where animals are less sensitive to those properties, and visually based behaviors. We then present the results wavelengths. of three new experiments that examine the effects of lighting envir- This paradox is potentially resolved when we consider that color onment on male/male competition, female mate choice, and preda- patterns can create high chromatic contrast without being particu- tion risk. We note that many studies examine the effects of lighting larly bright. In fact, similar phenomena have been noted in birds environments on female mating preferences (Long and Houde 1989; where brighter warbler species live in darker habitats (Marchetti Gamble et al. 2003; Maan et al. 2006; Maan and Cummings 2009), 1993), in sticklebacks where males with red throats are found in but few examine the effects of lighting environment on male/male clear water with high levels of blue scattering and are absent in red- competition. Of course, in many systems, male coloration is shifted waters (Reimchen 1989; Boughman 2001), in sticklebacks Downloaded from https://academic.oup.com/cz/article-abstract/64/4/499/5025950 by Ed 'DeepDyve' Gillespie user on 22 August 2018 Mitchem et al. Sensory drive in killifish 501 Figure 1. Blueﬁn killiﬁsh color morphs. (A) Blue color morph, (B) red color morph, (C) yellow color morph, (D) yellow–blue morph, (E) Red–blue morph, Figure 2. (A) The proportion of males that are blue in different populations as (F) female. Photos A, B, C, E by A. Terceira, photo D by B. Stauffer, photo E by a function of UV/Blue transmission (Fuller 2002); each dot shows the relative R.C.F. Note that blue males may also have yellow pelvic ﬁns and/or yellow abundance of blue males in a single population. (B) Swamp and spring water rear dorsal ﬁns. in white buckets. (C) The relative downwelling irradiance at 25.4 cm depth in a spring and a swamp. Curves are scaled to the maximum absolute irradi- ance. See Supplementary Figure 1a for absolute curves. (D) The average where blue opercle coloration increases with depth and red-shifted cone frequency in the eyes of animals from a spring and a swamp population light (Brock et al. 2017), in the cichlid species group Pundamilia (Fuller et al. 2003). (E) Proportional opsin expression for animals from a spring and a swamp (Fuller et al. 2004). where blue males are found in orange-tinted waters (Seehausen et al. 2008), and in surfperch where visual pigments match the ambient light spectrum yet visual signals are outside of the color realm of the brightness will be greatest when the shape of the reflectance spec- background light (Cummings and Partridge 2001; Cummings trum and the ambient light spectrum are similar but that contrasts 2007). In fact, in another seminal paper “The Color of Light in will be greatest when the shape of the reflectance spectra differs Forests and Its Implications”, Endler (1993b) predicted that total from the shape of the ambient light spectra. In the case of bluefin Downloaded from https://academic.oup.com/cz/article-abstract/64/4/499/5025950 by Ed 'DeepDyve' Gillespie user on 22 August 2018 502 Current Zoology, 2018, Vol. 64, No. 4 killifish, blue males most likely create high contrast against a tannin- stained water column. In addition, due to color constancy, individu- als may be particularly sensitive to blue wavelengths precisely be- cause they are rare. Color constancy is the phenomenon where the visual system differentially weights visual inputs to ensure that white is always perceived as white even under diverse illuminant (Cronin et al. 2014). In tannin-stained swamps with little UV/blue, individu- als must heavily weight the UV/blue inputs (i.e., the signals from the rare wavelengths) to create color constancy. This may create a situ- ation where swamp animals are particularly sensitive to UV/blue color signals. We note that this remains to be tested. We now turn our attention towards the effects of genetic variation and phenotypic plasticity with respect to lighting environments on male color pat- tern, opsin expression, foraging behavior, and mating behavior. The variation in male coloration is attributable to genetic vari- ation, phenotypic plasticity with respect to lighting environment, and genetic variation in phenotypic plasticity (Fuller and Travis 2004). All males have the ability to produce either yellow or red pterin, and crosses indicate that there is a locus of large effect where the yellow allele is dominant to the red allele (Fuller and Travis 2004; Johnson and Fuller 2015). When males are raised in clear water in the laboratory, they nearly all express red or yellow color- ation on their anal fins, and all males, regardless of lighting environ- ment, express red or yellow coloration on their pelvic fins (Fuller and Travis 2004). The coloration in the pelvic fins is perfectly corre- lated with the coloration in the anal fin. That is, males with red anal fins always have red pelvic fins, and males with yellow anal fins al- ways have yellow pelvic fins. Johnson and Fuller (2015) extracted pigments from the anal fins and analyzed them with spectroscopy. We showed that the red pterin is likely drosopterin, and yellow pterin is likely xanthopterin. Red males express both drosopterin and xanthopterin, whereas yellow males only express xanthopterin. However, the red/yellow anal fin coloration can be masked by the expression of blue. Blue expression has both genetic and environmental compo- nents. Fuller and Travis (2004) conducted a breeding study where they created paternal half-sib families and raised half of the off- spring in clear water, which mimics springs, and half of the offspring in tea-stained water, which mimics swamps. Note that throughout this article, we use the term “tea-stained” to refer to water, where we experimentally manipulated the lighting environment by adding instant tea. We use the term “tannin-stained” water to refer to water from nature that is naturally stained due to dissolved organic materi- als. Fuller and Travis (2004) showed that phenotypic plasticity favored blue males in tea-stained water. Specifically, blue sons were often produced in the tea-stained treatment but were rare in the clear water treatment (Figure 3A). There was also genetic variation in phenotypic plasticity. The sons of some sires were non-responsive to the variation in lighting environment. Hence, there was genetic Figure 3. (A) Sons are more likely to express blue coloration when raised in variation, phenotypic plasticity, and genetic variation in phenotypic tea-stained water. Genetic effects due to sires are also present (Fuller and plasticity. Subsequent studies have found that phenotypic plasticity Travis 2004). Each dot represents a clutch. (B) Opsin expression varies due to rearing environment (Fuller et al. 2005). (C) Killiﬁsh are more likely to peck at is also variable among populations (L.M., C. Chang, R.C.F., unpub- blue dots when raised and tested in tea-stained water (white bars ¼ clear test- lished result). Most important, the direction of phenotypic plasticity ing environment; dark bars ¼ tea testing environment) (Fuller et al. 2010). (D) favors the production of blue males in tea-stained water. Killiﬁsh from a variable lighting population only peck at blue when tested in Opsin expression is also influenced by both phenotypic plasticity tea-stained water and are more likely to peck at mid-day (Johnson et al. and genetic variation, but here there is little evidence for genetic 2013). (E) Preference for blue males is highest when swamp females are variation in phenotypic plasticity (Fuller et al. 2005a, 2010; Fuller raised and tested in tea-stained water (Fuller and Noa 2010). The graph shows and Claricoates 2011; Johnson et al. 2013). Lighting environments means from the tea-stained testing environment as a function of clear (open) and tea-stained (dark) rearing environments. The dotted line indicates the have large effects on opsin expression, where there is high propor- null expectation for no preference. tional expression of SWS1 (the opsin responsible for UV Downloaded from https://academic.oup.com/cz/article-abstract/64/4/499/5025950 by Ed 'DeepDyve' Gillespie user on 22 August 2018 Mitchem et al. Sensory drive in killifish 503 photopigment) in clear water and high proportional expression of These experiments examine the effects of lighting environments on RH2-1 and LWS (the opsins responsible for the green and red male competition, female mating preference, and predation. Of photopigment, respectively) in tea-stained water. The among popu- these three experiments, the male/male competition experiment is lation pattern of opsin expression (high SWS1 and SWS2B expres- genuinely novel. In bluefin killifish, male competition has a large in- sion in springs; high RH2-1 and LWS expression in swamps; fluence on the outcome of mating success (Mcghee et al. 2007; Figure 2C) can be largely recapitulated by raising animals in a green- Mcghee and Travis 2010, 2011; Johnson and Fuller 2015). Yet, few, house in either clear or tea-stained water (Figure 3B)(Fuller et al. studies have experimentally manipulated lighting environments to 2004, 2005a). In addition, there is good evidence that diurnal mimic natural conditions and subsequently found dramatic effects rhythms have very large effects on opsin expression (Johnson et al. on male/male competition. Our study below shows that lighting 2013). environments alter the outcome of male/male competition and favor Lighting environments also have multi-faceted effects on both the presence of blue males in swamps. foraging and mating preferences. Our group used a large breeding design to examine the roles of genetics (population of origin), rear- Materials and Methods ing environment (clear or tea), and testing environment (clear or tea) on foraging and mating preferences (Fuller and Noa 2010; Fuller To examine male/male competition in different lighting environ- et al. 2010). This allowed us to examine genetics, developmental ments, we placed male bluefin killifish with blue anal fins in trials plasticity as a function of lighting environment, and the immediate that varied in (a) lighting environment (clear versus tea-stained effects of lighting environment on visually based behaviors. For for- water) and (b) rival competitor color (males with solid yellow or red aging preferences, we dropped a clear petri dish to which we had anal fins). To examine female mating preferences, we performed no- attached different colored dots (red, orange, yellow, green, blue, choice mating assays where we placed a single female with either a black, white) into the water and counted how often the fish pecked red, yellow, or blue male under clear and tea-stained water condi- at each dot (Fuller et al. 2010). The fish pecked at these dots as if tions and measured the number of eggs produced. To examine the they were pecking at food. For foraging, there were no effects of roles of predators, we utilized a behavioral assay where largemouth genetics, but there were large effects of rearing environments. For bass could strike at different color morphs held in clear, plastic example, individuals were more likely to peck at red (and less likely boxes in either clear or tea-stained water. We describe these three to peck at yellow) dots when reared in tea-stained water. In add- experiments below. For simplicity, we only considered males with ition, there were strong interactions between rearing and testing en- solid blue anal fins and excluded males with combination red–blue vironment that suggested that lighting environments have strong or combination yellow–blue anal fins. Throughout the article, “tea- effects on the development of the visual system that result in differ- stained” refers to experimentally manipulated water in the lab. ent visually based behaviors depending on the immediate testing en- “Tannin-stained” refers to water in nature that is heavy in tannin vironment. Killifish pecked more at blue dots when they were raised levels and is typically found in swamps. and tested in tea-stained water (Figure 3C; Fuller et al. 2010). Another experiment used animals from a “variable” population (a Collection tannin-stained river adjacent to a clear spring) and tested pecking For the male competition and female mate choice studies, we col- preferences in clear and tea-stained water at dawn, mid-day, and lected bluefin killifish using dipnets and seines from a swamp popu- dusk (Johnson et al. 2013). That study found that killifish never lation (26-Mile Bend, Everglades Drainage, Broward Co., FL, USA) pecked at blue dots in clear water. Instead, they pecked at blue dots and a spring population (Guaranto Springs, Suwanee River in tea-stained water, particularly at mid-day (Figure 3D). Why these Drainage, Dixie Co., FL, USA). Guaranto Springs is unique because patterns emerge is unclear as bluefin killifish do not have blue food. it is a clear spring population that is connected to the Suwannee However, it is intriguing that preferences for blue inanimate objects River, which is tannin-stained during wet years. Upon collection, consistently arise in tea-stained treatments. fish were held in water from the site in coolers and immediately Finally, a complex interaction between genetics, rearing environ- transported to the lab at the University of Illinois at Urbana- ment, and testing environment affect female mating preference for Champaign. In the lab prior to experimentation, fish were main- blue males (Fuller and Noa 2010). Female mating preferences were tained in 114 L (29 gallon) tanks in a naturally lit, temperature con- measured in no-choice spawning assays where the number of eggs trolled greenhouse and fed frozen brine shrimp daily. Killifish laid with either blue, yellow, or red males in clear and tea-stained originating from the swamp population were kept in tea-stained water was taken as a measure of preference. Overall mating prefer- water. Killifish originating from the spring populations were kept in ences were weak, but the highest level of mating preferences for blue clear water. The maximum density of fish in a tank is 1 fish per 3.8 males were found in females from swamp parents that were raised L (1 gallon) of water. Both males and females were housed together and tested in tea-stained water (Figure 3E). The implication was that in stock tanks to prevent females from becoming egg bound. Hence, preference for blue males is only expressed when females have the females were housed with the male color morphs from their own right combination of genetics, rearing environment, and testing en- populations. Stock tanks were regularly monitored, and fish had ac- vironment (Fuller and Noa 2010). cess to naturally occurring algae and invertebrates. Killifish were The patterns of genetic variation, phenotypic plasticity, and gen- allowed to acclimate to the laboratory for two weeks before begin- etic variation in phenotypic plasticity across multiple traits favor the ning behavioral assays. presence of blue males in swamps. However, less is known about the selective forces at play in this system. Our previous work indi- cated that female preference may favor blue males in swamps, but Male competition the effects were small. Little is known about the effects of lighting Our goal was to determine the effect of male anal fin coloration on environments on male/male competition or predation. Below, we the outcome of male/male competition and whether this varied as a present the results of three new experiments that fill in these gaps. function of lighting environment. To do this, we allowed two males Downloaded from https://academic.oup.com/cz/article-abstract/64/4/499/5025950 by Ed 'DeepDyve' Gillespie user on 22 August 2018 504 Current Zoology, 2018, Vol. 64, No. 4 to compete in the presence of one female in either clear water, which swamp mean ¼ 26.8 mm, spring mean ¼ 25.4 mm). While there was mimics springs, or tea-stained water, which mimics swamps, and no systematic difference in size among the color morphs, we found determined the effect of anal fin coloration on male dominance in that blue males were more likely to emerge as dominant when they different environmental lighting conditions. We used Lipton Instant were larger than their competitors. We therefore included the differ- decaffeinated tea powder to create tea-stained water. We periodical- ence in size between the blue male and the competitor as a covariate ly added tea to the tanks so that the water mimicked the appearance in all of our models. of iced tea. This was necessary because bacteria degrade the tea in We tested whether the likelihood of blue males emerging as dom- the water. The same phenomenon occurs in natural populations inant and courting females was affected by lighting environment where bacteria consume dissolved organic materials. The addition (clear or tea-stained), the color of the competing male (red or yel- of instant tea to the water mimics the natural lighting environments low), population of origin (spring or swamp), their interactions, or of swamps (see bass predation experiment below, Figure 2C, the difference in size between the two males. We analyzed four vari- and Supplementary file 1 A–B for representative irradiance spectra ables. We first analyzed whether the focal male was dominant or for quantification of irradiance). We used UV sterilizers to remove subdominant. We also considered the proportion of aggression that algae and bacteria from the water column to maintain our treatment was performed by the blue male in each trial. We next tested effects. whether dominance translated into mating opportunities. We ana- We selected eight blue color morphs from each population to use lyzed (a) the proportion of courtship performed by the blue male as focal males. For each trial, the focal male was paired with a com- compared to the total courtship performed by both males and petitor male (either a red or yellow male) and a female from the (b) the proportion of time that the blue male spent within 1 body same population. Each focal male was paired with each color morph length of the female compared to the total time that either male (red and yellow) in clear and tea-stained water resulting in 4 trials spent within 1 body length of the female. Trials were excluded from per male (2 competing color morphs 2 lighting environments ¼ 4 the analysis if no courtship was performed (4 trials) or if neither trials per focal male). One focal male from the spring population male spent time close to the female (2 trials). The focal male identity died after completing only three trials. A total of 63 trials were con- (ID) was treated as a random effect in all four analyses (blue male ducted (8 males 2 populations 2 lighting treatments 2 color dominance, blue male aggression, blue male courtship, and blue morph competitors minus one missing trial). The order of the pair- male percentage time near the female). For all four analyses, we ini- ings (red or yellow competitor) and light treatments (clear or tannin- tially used the following model: dependent variable lighting envir- stained) were randomized for each male. Male ID was treated as a onment (LE) þ competitor color pattern (CP) þ population of origin random effect in subsequent analyses. (Pop) þ LE*CP þ LE*Pop þ CP*Pop þ LE*CP*Pop þ size difference Before beginning trials, we separated males into 38 L aquaria þ (1jID). However, for the analysis of male dominance status, the and visually isolated them from all other fish. Trials occurred in full model failed to converge. We then removed the interaction 114 L aquaria with naturally occurring algae and invertebrates. terms and re-ran the analysis. For the other three variables (propor- Each tank contained yarn mops (i.e. several 12-inch pieces of yarn tion of aggression, proportion of courtship, proportion of time near tied together) which served as spawning substrates. The spawning the female), the full models converged. For all four analyses, we per- substrates were attached to either Styrofoam balls so that they formed a type 3 analysis using the “car” package to examine the floated or to small pieces of PVC pipe so that they sunk. The spawn- effects of each model term. The analysis of blue dominance assumed ing substrates provided a place for fish to attach eggs and also pro- a binomial distribution and used the “glmer” function. The analyses vided refuge to hide from other aggressive fish. of proportions (aggression, courtship, time) used linear models The first author observed each set of killifish once each day for assuming normal distribution of errors. For these analyses, we used twenty minutes between the hours of 08:00 and 12:00 for 3 consecu- the “lmer” function in the “lme4” package in R. The advantage of tive days and recorded the number of male aggressive behaviors dur- performing the analyses on the proportions is that it avoids overdis- ing each observation period. These behaviors included: fin flares, persion. We visually inspected the plots of the residuals against the chases, and attacks resulting in physical contact towards the com- predicted values and normal Q–Q plots to check for heteroscedastic- peting male and stimulus female (noted as aggressive behaviors in: ity. We also performed Levene’s test and found no evidence for het- Johnson and Fuller 2015). We used the aggressive behavior counts eroscedastic variances. to determine male dominance. The male who performed the most aggressive acts was noted as dominant. The males typically estab- lished dominance relationships within the first day. No males Female preference reverted between dominant and subdominant status during the 3 To determine the effect of anal fin coloration on female mate choice, days. We also recorded courtship behaviors as the time spent within we allowed one female and one male to spawn together for 5 consecu- one body length of the stimulus female, the number of courting tive days in either clear or tea-stained water. Each focal female was bouts (head flicks and body loops towards female), and the number paired with all three color morphs (blue, red, yellow) in both clear and of spawns. Due to low numbers of observed spawns, we did not con- tea-stained environments across six weeks of trials. Each pairing with sider this variable further. Following the completion of all behavior- a male lasted 5 days. We then gave females a two-day resting period. al assays, fish were euthanized using an overdose of buffered MS- The next week, we paired the female with another male. The order of 222. treatments (i.e., male color and light treatments) were randomized for We calculated standard length (from the tip of the snout to the each female. We created tea-stained and clear treatments using the caudal peduncle) for every fish in every trial. Standard length did same methods used in the male competition trials. not differ among color morphs (F ¼ 2.41, P ¼ 0.10) or as an For each weekly trial, we placed mating pairs in 34 L aquaria 2,39 interaction between color morph and population (F ¼ 1.72, containing spawning substrates (i.e., yarn mops) at night and 2,39 P ¼ 0.19), but it did differ between populations where the swamp allowed them to spawn for the ensuing 5 days. We used the number fish were slightly larger than spring fish (F ¼ 5.56, P ¼ 0.024, of eggs produced as a measure of female preference. This is a “no- 1,39 Downloaded from https://academic.oup.com/cz/article-abstract/64/4/499/5025950 by Ed 'DeepDyve' Gillespie user on 22 August 2018 Mitchem et al. Sensory drive in killifish 505 choice” assay which we have successfully used in past studies of sex- depth in four of our tanks (FL bass and IL-Hatchery) at noon on ual selection and speciation (Fuller and Noa, 2010; Kozak et al. July 3, 2013. We did not measure light in the IL-Wild tanks because 2015; St John 2017). One of us (L.D.M.) searched the spawning they had already been taken down when we took the data. We used substrates each day, counted the eggs, and then subsequently dis- an OceanOptics 2000 spectrophotometer connected to a patch cord carded them. and a cosine corrector. The spectrophotometer, patch cord, and co- We originally selected 9 females from both the spring and swamp sine corrector had been calibrated using a calibrated using a populations, but 1 spring female died after 3 weeks, leaving us with DH2000 (Deuterium–Halogen, Ocean Optics) light source. One of 8 spring females that had been paired in all 6 combinations. Hence, us (S.S.) held the probe upward in the water at the appropriate depth there were a total of 102 trials (6 treatments * 17 females). (25.4 cm), while another (R.C.F.) took measurements using a laptop Following the completion of all mating trials, fish were euthanized and SpectraSuite Software. For each tank, we calculated the relative using an overdose of MS-222. This experiment ran from August 15, down-welling irradiance as the absolute irradiance divided by the 2016 to September 23, 2016. maximum value for a given spectrum. The dependent variable was the total number of eggs laid. We per- For the predation assays, we placed individual killifish in clear formed a fully factorial analysis that considered the effects of lighting plastic boxes in the cattle tank for two minutes and counted the environment, male color, population, and their interactions. We number of times the bass struck the box. We tested each color treated female identity as a random factor. We used the ‘lme4’ pack- morph (blue, yellow, or red) singly at three separate times (morning, age in R with the ‘lmer’ function. We used a type 3 analysis of vari- mid-day, and dusk) on three separate days. Hence, each tank was ance to assess the effects of our treatments. We used Levene’s test and tested 27 times. To analyze the data, we considered the fixed effects visually inspected the residuals to check for heteroscedastic variances. of color morph (blue, yellow, red), population (Florida Everglades, Illinois Wild, Illinois Hatchery), time (morning, mid-day, dusk), lighting environment (clear or tea), and their interactions on the Preliminary predation number of strikes directed at the fish in the plastic boxes. Time of The goal of this study was to determine if predation risk varies be- day had no significant effect, so it was removed and not considered tween blue, yellow, and red males as a function of lighting environ- further. There were large differences among the populations in the ment. We used largemouth bass as the predator. Largemouth bass propensity of the bass to strike the boxes. We ran the same analysis are in all of our study populations in Florida (Fuller and Noa 2008), excluding the Illinois Wild bass (which were much less likely to and R.C.F. has observed them preying on bluefin killifish in nature. strike the boxes than either Illinois Hatchery or Florida Everglades), We used bass from three populations: Florida Everglades (26 Mile- and another analysis on just the Florida Everglades bass. The latter Bend, Broward Co., FL, USA), an Illinois Wild Population (Lake analysis was warranted because these bass co-occur with the killifish Shelbyville, Moultrie Co., FL, USA), and an Illinois Hatchery in nature in Florida. We ran a linear model in R using the “lm” func- (Jake Wolfe Hatchery, Mason Co., FL, USA). Largemouth bass tion and analyzed the treatment effects using a type 3 analysis in the were previously considered to be one wide-ranging species with mul- “car” package. These results should be considered preliminary due tiple subspecies, but have now been described as separate species to the fact that there were a limited number of tanks that were tested (Kassler et al. 2002). The Florida Everglades bass were, therefore, repeatedly. We used Levene’s test and visually inspected plots of the Florida bass Micropterus floridanus, while the Illinois Wild and residuals against the predicted values to check for heteroscedasticity. Illinois Hatchery bass were northern largemouth bass Micropterus Data for all three experiments have been deposited in Dryad salmoides. These two species do not differ in the spectral properties (doi:10.5061/dryad.3mn5rk4). of their cone cells (Mitchem et al. 2018). The Florida Everglades bass were collected with a bag seine; the Illinois Wild bass were collected via electroshocking from a boat; Results the Illinois Hatchery bass were provided by the Jake Wolfe Hatchery. For simplicity, we refer to these as three separate Male competition “populations”. The fish were transported back to the University of Blue males emerged as dominant more often in tea-stained treat- Illinois in aerated coolers. The fish were fed a mix of bass pellets ments (Figure 4; Table 1, v ¼ 4:94, P ¼ 0.026). In 25 out of 32 tri- and live feeder fish. We also collected male bluefin killifish of differ- als conducted in tea-stained water, blue males were dominant over ent color morphs, which served as the prey targets, from the Delk’s the competitor male (binomial probability¼ 0.002 where the null Bluff boat ramp (Marion Co., FL, USA) using seines and dipnets. expectation is a 50% probability of emerging as dominant). Blue These fish were also transported back to the University of Illinois males emerged as dominant in 16 out of 31 trials conducted in clear and housed in aquaria and cattle tanks. water conditions (binomial probability¼ 1). Differences in body size Two cattle tanks were established for each type of bass (4–5 bass also affected the outcome where blue males were more likely to per tank) for a total of six cattle tanks. For each population, one cat- emerge as dominant when they were larger (v ¼ 5:82; P ¼ 0.016). tle tank was established with clear water conditions, and another The same pattern of blue males emerging as dominant appeared to with tea-stained conditions. UV sterilizers were used to prevent be present in both populations (Figure 4). Nearly identical results algae blooms in the water column and maintain the lighting treat- were obtained when we considered the proportion of aggressive acts ments. Cattle tanks also had biological sponge filters connected to performed by blue males versus their competitors (Table 2, air pumps that removed nitrogenous waste from the tanks. F ¼ 5.75, P ¼ 0.021). Blue males performed a higher proportion 1,38.2 As with our male competition and female choice experiments of the aggressive acts in tea-stained water, and this was particularly (see above), we periodically added instant tea so that the tea-stained so for males from the swamp population (Figure 5A). Blue males treatments resembled the appearance of iced-tea. This is necessary were also more likely to be more aggressive when they were larger because over time the staining decreases due to bacterial decompos- than their competitors (Table 2, F ¼ 5.73, P ¼ 0.021). 1,46.9 ition of the tea. To verify that our treatments genuinely affected the The ability of blue males to court females and to remain in close light spectrum, we measured the down-welling irradiance at 25.4 cm proximity to females reflected the patterns in male dominance Downloaded from https://academic.oup.com/cz/article-abstract/64/4/499/5025950 by Ed 'DeepDyve' Gillespie user on 22 August 2018 506 Current Zoology, 2018, Vol. 64, No. 4 Figure 4. The frequency with which blue males emerged as dominant (“blue wins”) versus subdominant (“blue loses”) in trials as a function of population and lighting environment. Blue males are more likely to be dominant in tea- stained treatments. Table 1. Type 3 analysis of deviance (Wald v tests) on the domin- ance status of blue males. For each pairing, males were socred as either dominant (‘blue wins’) or subdominant (‘blue loses’). Inclusion of the interactions among the ﬁxed terms prevented the model from converging. Term v df P Intercept 1.44 1 0.230 Lighting environment 4.94 1 0.026 Population 1.90 1 0.168 Competitor color pattern 0.30 1 0.584 size difference 5.82 1 0.016 Table 2. Type 3 analysis of variance table (Wald F-tests with Kenward–Roger df) on the proportion of aggressive behaviors per- formed by blue versus competitor males Term Fdf (num, denom) P Intercept 105.38 1, 17.4 0.000 Lighting environment (LE) 5.75 1, 38.2 0.021 Population (Pop) 3.52 1, 14.5 0.081 Competitor color pattern (CP) 0.22 1, 37.6 0.641 Figure 5. The proportion of aggression (A), courtship (B), and time near the Size difference 5.73 1, 46.9 0.021 female performed by the blue male versus the competing male as a function LE * CP 0.55 1, 35.1 0.465 of lighting environment and population (C). Means6 SE. N ¼ 16 for all means LE * Pop 0.00 1, 38.3 0.954 except for the clear-spring treatment combination (N ¼ 15). CP * Pop 2.18 1, 40.6 0.147 LE*CP*Pop 2.78 1, 35.5 0.104 Female preference Females displayed no overall preference for any color morph be- tween lighting treatments (Figure 6). More eggs were collected from females in tea-stained environments (F ¼ 4.77, P ¼ 0.032), but (Table 3A–B). Blue males were more likely to court and to remain in 1,75 there were no differences in the number of eggs laid as a function of close proximity to females in tea-stained compared to clear water color morph nor as an interaction between color morph and lighting conditions (Figure 5B–C, courtship: F ¼ 8.47, P ¼ 0.006; time 1,35.8 environment (Table 4). Similarly, there was no difference in female near female: F ¼ 10.54, P ¼ 0.003). Furthermore, blue males 1,36.3 preference between populations. from swamps were particularly likely to have an advantage in court- ing and remaining close to females in tea-stained conditions (popula- tion effect courtship: F ¼ 6.01, P ¼ 0.028; time near female: 1,14.3 F ¼ 5.68, P ¼ 0.031). Likewise, blue males from springs were at Preliminary predation 1,14.4 a disadvantage in clear water. Blue males were also more likely to The addition of instant tea dramatically decreased the amount of court females when they were larger than their competitors (F blue and UV light (380–550 nm) available in the tanks (Figure 7A, 1,40.4 ¼ 6.19, P ¼ 0.017), but the effect of size was marginal for the time Supplementary Figure 1B). These results are similar to those seen in spent near females (F ¼ 2.92, P ¼ 0.094). the wild (Figures 2C and 7A) with the notable exception that the UV 1,43.2 Downloaded from https://academic.oup.com/cz/article-abstract/64/4/499/5025950 by Ed 'DeepDyve' Gillespie user on 22 August 2018 Mitchem et al. Sensory drive in killifish 507 Table 3. Type 3 analysis of variance (Wald F-tests with Kenward– Roger df) for the proportion of courtship performed by the blue male versus the competitor male (A) and the proportion of time spent near the female by the blue male versus the competitor male (B). A. Blue Courtship Effect Fdf (num, denom) P (Intercept) 132.78 1, 16.4 0.000 Lighting environment (LE) 8.47 1, 35.8 0.006 Population (Pop) 6.01 1, 14.3 0.028 Competitor color pattern (CP) 1.82 1, 36.0 0.186 Size difference 6.19 1, 40.4 0.017 LE * Pop 0.42 1, 36.3 0.521 LE * CP 0.03 1, 35.6 0.868 CP * Pop 0.16 1, 38.9 0.695 LE*CP*Pop 1.29 1, 36.2 0.264 B. Time near female by blue male Effect Fdf (num, denom) P Intercept 123.77 1, 16.8 0.000 Lighting environment (LE) 10.54 1, 36.3 0.003 Population (Pop) 5.68 1, 14.4 0.031 Competitor color pattern (CP) 0.41 1, 36.6 0.526 Size difference 2.92 1, 43.2 0.094 LE * Pop 0.01 1, 36.6 0.941 LE * CP 0.17 1, 34.4 0.684 Pop * CP 0.57 1, 40.1 0.453 LE * CP *Pop 0.91 1, 34.9 0.347 wavelengths below 380 nm are absent due to the filtering properties Figure 6. The total eggs spawned as a function of male color and lighting en- of the greenhouse. vironment for (A) spring and (B) swamp ﬁsh. Preliminary evidence suggests that blue males may suffer a lower risk of predation in tea-stained water compared to clear water. The Table 4. Type 3 analysis of variance (Wald F-tests with Kenward– initial analysis including all three populations of bass (Florida Roger df) on the number of eggs spawned by females as a function Everglades, Illinois Hatchery, Illinois Wild) found a marginally sig- of lighting environment, population, and male coloration nificant interaction between lighting environment and male color Term Fdf (num, denom) P morph (Table 5A, F ¼ 5.25, P ¼ 0.086). There was also a large 2,144 overall effect due to population (F ¼ 20.17, P ¼ 0.001) that was 2,144 (Intercept) 161.95 1, 15 <0.001 caused by Illinois Wild bass striking the boxes less often than the Lighting environment (LE) 4.77 1, 75 0.032 Illinois Hatchery and Florida Everglades Bass [Table 5A, P < 0.001; Population (Pop) 1.37 1, 15 0.260 Male Color 2.03 2, 75 0.139 Illinois Wild: 7.46 1.3 (SE) strikes; Illinois Hatchery: 16.86 1.7 LE Pop 1.91 1, 75 0.171 (SE) strikes, Florida Everglades: 18.46 (1.4 SE) strikes]. Removing LE Color 0.75 2, 75 0.475 the Illinois Wild Bass from the analysis resulted in a significant inter- Pop Color 1.15 2, 75 0.323 action between lighting environment and male color morph LE Pop Color 0.08 2, 75 0.928 (Table 5B, F ¼ 3.60, P ¼ 0.031), where blue males were less like- 2,96 ly to receive strikes in tea-stained water compared to clear water (Figure 7). An analysis restricted solely to the Florida Everglades Bass also results in a marginally significant interaction between compared to clear water. Third, in contradiction to our previous lighting environment and male color morph (Table 5C, F ¼ 3.14, work (Figure 3E), we found no evidence that female mating prefer- 2,48 P ¼ 0.052). Supplementary Figure 2 shows the interaction between ences favor blue males in swamps. Below, we discuss the implica- male color morph and lighting environment for each population. tions of these three results and then discuss the broader importance for the bluefin killifish system. Discussion Male competition Three main findings emerge from these experiments. First, the out- Our study provides direct evidence that lighting environments alter come of male/male competition varies depending on lighting envir- the outcome of male/male competition where blue males are favored onment where blue males are more likely to be dominant in tea- in tea-stained water. Previous work indicates that the outcome of stained water. Second, preliminary studies using bass indicate that male/male competition has an overwhelming influence on the actual blue males may be less susceptible to predation in tea-stained water outcome of mating (Mcghee et al. 2007; Mcghee and Travis 2010, Downloaded from https://academic.oup.com/cz/article-abstract/64/4/499/5025950 by Ed 'DeepDyve' Gillespie user on 22 August 2018 508 Current Zoology, 2018, Vol. 64, No. 4 Table 5. Type 3 analysis of variation of the effects of lighting envir- onment (LE), population (pop), and male color (color) on the num- ber of bass strikes at red, yellow, and blue males in clear plastic boxes. (A) All three populations. (B) Florida everglades and Illinois hatchery ﬁsh. (C) Florida everglades bass. A. All three populations. Term Fdf (num, denom) P (Intercept) 342.97 1, 144 < 0.001 Lighting Environment (LE) 27.06 1, 144 < 0.001 Population (Pop) 20.17 2, 144 < 0.001 Male Color 2.00 2, 144 0.140 LE Pop 5.25 2, 144 0.006 LE Color 2.49 2, 144 0.086 Pop Color 1.54 4, 144 0.195 LE Pop Color 0.72 4, 144 0.582 B. Illinois Hatchery and Florida Everglades Populations Term Fdf (num, denom) P Intercept 354.94 1, 96 < 0.001 Lighting Environment (LE) 37.23 1, 96 < 0.001 Population (Pop) 0.69 1, 96 0.407 Figure 7. (A) Relative down-welling irradiance at 25.4 cm depth in clear and Male color 1.07 2, 96 0.348 tea-stained treatments. Each curve is scaled by the maximum down-welling LE Pop 0.48 1, 96 0.490 irradiance. See supplemental ﬁgure 1 for absolute irradiance spectra. (B) The LE Color 3.60 2, 96 0.031 effects of lighting environment and male color on the number of bass strikes Pop Color 2.15 2, 96 0.122 over 2 min for the Florida Everglades and Illinois Hatchery bass pooled. LE Pop Color 0.30 2, 96 0.743 Means6 SE. N ¼ 18 for each bar. C. Florida Everglades 2011). Hence, the results of this experiment suggest that blue males Term Fdf (num, denom) P have a genuine fitness advantage in swamps. We see two potential Intercept 244.77 1, 48 <0.001 explanations as to why this occurs. The first is that, like female Lighting environment (LE) 18.50 1, 48 <0.001 choice, visual contrasts play an important role in male/male compe- Color 0.89 2, 48 0.417 tition. Conspicuousness (i.e., chromatic and/or achromatic con- LE Color 3.14 2, 48 0.052 trasts) have long been assumed, and sometimes shown, to be important to female mating preferences (Pauers et al. 2004; Gray et al. 2008; Maan and Cummings 2009; Kemp et al. 2009; Dalton et al. 2010; Morehouse and Rutowski 2010; Tanaka et al. 2011; Ronald et al. 2012). These contrasts might reduce search costs for predation risk in clear water and low predation risk in swamps (see females, advertise male health and genetic quality, or appeal to arbi- below), and that their willingness to engage in competition reflects trary preferences that have been shaped by evolutionary forces such these effects. In this case, blue males have an advantage in swamps as natural selection on sensory system properties, Fisherian sexual because they are more willing to engage in extended, conspicuous selection, or past evolutionary history (Fuller et al. 2005b; Ryan and displays in tea-stained water in comparison to other color morphs. Cummings 2013). Do these same principles apply to the signals This hypothesis predicts that there should be different levels of risk males use in male/male competition? With competition, signals are taking between the color morphs as a function of the lighting often “put to the test”. Individuals signal to one another, but if dis- environment. putes cannot be resolved via signaling, then they escalate to costly fighting (Tibbetts and Dale 2004; Searcy and Nowicki 2005; Tibbetts and Izzo 2010). Our previous work using spring fish in Preliminary predation clear water indicates that similar phenomena occur in bluefin killi- Our preliminary evidence suggests that blue males may be less sus- fish where melanin serves as a badge of status (Johnson and Fuller ceptible to predation in swamps than in springs. We consider these 2015). Blue coloration may serve a similar function in swamp habi- results to be preliminary because we repeatedly tested 6 cattle tanks tats. The blue anal fin may conceivably create high contrast with the of bass (3 populations 2 lighting treatments). Ideally, we would water column. This explanation predicts that high contrast males have used multiple cattle tanks per treatment, but logistical con- should emerge as dominant more often than low contrast males and straints prevented this. Other preliminary studies examining the that contests between males with similar levels of contrast should be likelihood of bass to strike at different inanimate objects that resem- long and costly. These hypotheses are testable with detailed observa- ble food suggest increased strike rates at blue objects in clear water tions, visual detection models, and experiments that directly ma- (S. Feng, N. Karin, R.C.F., unpublished data). If these results hold, nipulate contrast. A second hypothesis is that blue males alter their then they indicate that the direction of selection via predation is the competitive behavior in clear versus tea-stained water as a function same as the direction of selection via male/male competition. This is of predation risk. This hypothesis assumes that blue males face high in contrast to other systems where the direction of selection via Downloaded from https://academic.oup.com/cz/article-abstract/64/4/499/5025950 by Ed 'DeepDyve' Gillespie user on 22 August 2018 Mitchem et al. Sensory drive in killifish 509 sexual selection opposes the direction of selection via predation/nat- compared female choice for males with different color patterns with ural selection (Endler, 1995). the outcome of male/male competition and found that females mated Exactly why these effects occur is unclear. One possibility is that rapidly when preferred males were dominant, but had a longer latency color patterns appear different to conspecifics than they do to preda- to mate when preferred males were subdominant. Clearly, there is tors (Siddiqi et al. 2004; Bybee et al. 2012; Crothers and Cummings good evidence that natural variation in lighting environments is corre- 2013), creating the opportunity for animals to signal in a private lated with changes in male coloration and that female mating preferen- channel. The visual system of the bass is quite different from that of ces are associated with many of these patterns (e.g., guppies: Endler the bluefin killifish. Largemouth and Florida bass possess only two and Houde, 1995; cichlids: Seehausen et al. 2008; Maan and cones in their retinas that are sensitive to longer wavelengths (k Seehausen 2010; Maan et al. 2010; Telemantheria: Gray et al. 2008; max values of 535 nm and 614 nm) (Mitchem et al. 2018). In contrast, sticklebacks: Reimchen 1989; Mckinnon, 1995; Boughman 2001; bluefin killifish have at least five cone classes with spectral sensitiv- surfperch: Cummings 2007). Yet, the roles of lighting environment on ity extending into the UV but less in the far-red region (k values the interaction between male competition and female choice remains max of 359 nm, 405 nm, 455 nm, 537 nm, and 573 nm) (Fuller et al. unclear in many systems. 2003). These different visual sensitivities may set up a scenario where ‘blue’ signals serve as a private communication channel in The bluefin killifish system tannin-stained waters. These signals might travel over the short dis- We contend that bluefin killifish provide some of the best evidence tances required for signaling with conspecifics (0.5 m) but attenu- for Endler’s theory of sensory drive (Endler 1992, 1993a). The dif- ate or appear more cryptic to bass over the longer distances at which ferences in lighting environments between clear springs and tannin- predators view them. Clearly, we are not the first to suggest such dy- stained swamps set the stage for the evolution of male color pat- namics. Private communication channels have been suggested for terns, sensory system properties, non-mating behaviors (e.g., forag- many groups including swordtail fish (Cummings et al. 2003), elec- ing), and mating behaviors (male/male competition). Furthermore, tric fish (Arnegard et al. 2010), and moths (White et al. 2015). In all the direction of phenotypic plasticity in male color patterns (where of these systems, sensory properties of the predators dictate the sen- males are more likely to express as blue when raised in tea-stained sory space (i.e., range of wavelengths and frequencies) and modal- water) and foraging preferences (animals peck at blue dots in tea- ities that animals use for signals. stained water) suggest that the direction of phenotypic plasticity coincides with the direction of selection. Lighting environments not Female mate choice only affect the direction of selection and genetic differentiation Our previous work indicated that females had weak preferences for among populations, they also influence the development of traits in blue males provided that they came from swamp parents, were raised a putatively adaptive fashion. Again, bluefin killifish provide some in tea-stained conditions, and were tested in tea-stained water. Our of the best evidence for sensory drive due, in part, to the very dra- previous work also found preference for red males for females from matic differences among lighting habitats. spring parents (Fuller and Noa 2010,see also Fuller and Johnson While this system is ripe for multiple future avenues of research, 2009; Johnson et al. 2018). We did not repeat these patterns here. we argue that there are two areas that stand out. First, while the Both studies used no-choice female choice assays which are thought to bluefin killifish provides strong evidence for sensory bias from an eco- be conservative (Houde 1997, but see St John 2017). However, there logical genetics standpoint, we have very little understanding mechan- were some differences in methodology. The previous assays (Fuller istically of why blue males are favored in swamps and disfavored in and Noa 2010) were conducted in a fish room with good temperature springs. The patterns presented here beg for a proper analysis via vis- control but artificial light, whereas the current study was conducted in ual detection models (Vorobyev and Osorio 1998; Vorobyev et al. a greenhouse with much greater thermal fluctuations, but natural 1998; Kemp et al. 2015). Visual detection models will allow us to ask light. The previous study also only considered egg production over a whether blue males possess higher contrast than red or yellow males 4-h period, whereas the current study considered egg production over when viewed by conspecifics in tannin-stained water and whether they 1 week. However, we still obtain no pattern of preference even if we are less conspicuous to bass. The bluefin killifish-bass system is excel- limit our analyses to the eggs laid on day 1. The previous study used lent for constructing and testing visual detection models due to our lab-reared animals whereas the current study used field-caught indi- ability to readily manipulate lighting environments, color patterns, viduals. Why these differences in methodology should cause thee dif- and visual system properties. Visual detection models will also allow ferent patterns is unclear. The other explanation is that female us to ask why blue males are absent from springs and whether they are preferences for different male color morphs are weak. While we have more conspicuous to predators and/or conspecifics. not demonstrated strong preferences for different color morphs, we The second glaring question is what maintains the variation in have demonstrated strong patterns of female mating preference in our male coloration? All of our study populations in Florida have mul- speciation work (Gregorio et al. 2012; Kozak et al. 2015; St John tiple color morphs. Like the situation with guppies, there are stag- 2017). We have repeatedly shown that females and males that occur gering levels of variation in male coloration within populations, and in sympatry with a close relative, the rainwater killifish L. parva,have we do not understand how these are maintained. These color heightened levels of preference compared to allopatric animals. morphs do not represent different alternative mating strategies. Furthermore, females that co-occur with rainwater killifish also have There are no sneakers and all males compete to guard females and heightened preferences for males from their own populations over for- patches of vegetation away from other males. They do not differ in eign populations. The relevant point for this article is that we can re- body size nor in age at sexual maturation. peatedly show patterns of preference provided that preferences are How can such high levels of variation be maintained? Spatial strong. We suspect that preferences for males with different color pat- and temporal variation in lighting environments may play a role in terns are weak and are often superseded by the outcome of male/male this system. In the Suwanee, St John’s, and Withlacootchee river competition (see Berglund et al. 1996 for a discussion of traits used in drainages, there are spring populations that connect to tannin- male competition and female choice). In fact, Mcghee et al. (2007) stained rivers, which create dramatic spatial variation. There is also Downloaded from https://academic.oup.com/cz/article-abstract/64/4/499/5025950 by Ed 'DeepDyve' Gillespie user on 22 August 2018 510 Current Zoology, 2018, Vol. 64, No. 4 Braun C, Michiels NK, Siebeck UE, Sprenger D, 2014. Signalling function of temporal variation due to droughts and extreme rain across years. long wavelength colours during agonistic male–male interactions in the Another possibility is that there is microhabitat variation with re- wrasse Coris Julis. Marine Ecol Progress Series 504:277–286. spect to either depth or diurnal rhythms. Both theory and empirical Brock CD, Cummings ME, Bolnick DI, 2017. Phenotypic plasticity drives a work indicate that variation in lighting habitats may allow for the depth gradient in male conspicuousness in threespine stickleback maintenance of different color morphs (Endler 1987; Endler 1993b, Gasterosteus Aculeatus. Evolution 71:2022–2036. Schluter and Price 1993; Chunco et al. 2007; Gray et al. 2008; Buchinger TJ, Bussy U, Li K, Wang H, Huertas M et al., 2017. Phylogenetic Hurtado-Gonzales et al. 2014). Our previous work on foraging pref- distribution of a male pheromone that may exploit a nonsexual preference erences provided support for the idea that color-based preferences in lampreys. J. Evol. Biol. 30:2244–2254. vary over the course of the day (Johnson et al.2013). Whether such Bybee SM, Yuan FR, Ramstetter MD, Llorente-Bousquets J, Reed RD et al., effects extend to male-male competition (or the ever fleeting female 2012. Uv photoreceptors and Uv-yellow wing pigments in Heliconius but- terﬂies allow a color signal to serve both mimicry and intraspeciﬁc commu- mating preferences) is unknown. nication. Am Nat 179:38–51. In conclusion, bluefin killifish provide exceedingly strong sup- Chunco AJ, Mckinnon JS, Servedio MR, 2007. Microhabitat variation and port for sensory drive. Differences between clear water and tannin- sexual selection can maintain male color polymorphisms. Evolution 61: stained lighting environments affect nearly every aspect of the sen- 2504–2515. sory drive process. Our review showed strong among population Cronin TW, Marshall NJ, Caldwell RL, 1996. Visual pigment diversity in two patterns in signals, visual systems, and visually-based behaviors at- genera of mantis shrimps implies rapid evolution (Crustacea: stomatopoda). tributable to variation in the lighting environment via genetic vari- J. Comp Physiol 179:371–384. ation, phenotypic plasticity as a function of the lighting Cronin TW, Caldwell RL, 2002. Tuning of photoreceptor function in three environment, and genetic variation in phenotypic plasticity. Our mantis shrimp species that inhabit a range of depths. Ii. Filter Pigments. three new experiments provided sorely needed data concerning the J. Comp. Physiol. 188:187–197. Cronin TW, Johnsen S, Marshall NJ, Warrant EJ, 2014. Visual Ecology. direction of selection via male/male competition, female mate Princeton: Princeton University Press. choice, and predation. We found strong evidence that differences in Crothers LR, Cummings ME, 2013. Warning signal brightness variation: sex- lighting environments alter the direction of competition where blue ual selection may work under the radar of natural selection in populations males are favored in tea-stained water but not in clear water. In con- of a polytypic poison frog. Am Nat 181:E116–E124. trast to previous work, we found no evidence for female mating Crothers LR, Cummings ME, 2015. A multifunctional warning signal behaves preferences in any lighting environment. Finally, preliminary evi- as an agonistic status signal in a poison frog. Behav Ecol 26:560–568. dence suggests that blue males might experience lower predation Cummings ME, Partridge JC, 2001. Visual pigments and optical habitats of surfperch risks in tea-stained water than they do in clear water. The emerging (Embiotocidae) in the California kelp forest. J. Comp. Physiol. 187:875–889. pattern is one where the direction of selection due to male/male Cummings ME, Rosenthal GG, Ryan MJ, 2003. A private ultraviolet channel competition, the direction of selection due to predation, the nature in visual communication. Proc. Roy. Soc. Lond B Biol Sci 270:897–904. Cummings ME, 2007. 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