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Sensory drive in colourful waters: morphological variation suggests combined natural and sexual selection in an Amazonian fish TIAGO H. S. PIRES", ELIO A. BORGHEZAN’?, SERGIO L. R. CUNHA13, RAFAEL P. LEITAO. KALEBE S. PINTO’ and JANSEN ZUANON’ `Laboratorio de Ecologia Comportamental e Evolutiva – LECE, Instituto Nacional de Pesquisas da Amazonia – INPA. Au. Andre Araujo, 2936 – Petropolis, Manaus AM, Brazil Wildlife Research Center of Kyoto University., 2-24 Tanaka-Sekiden-cho, Sakeyo-ku, Kyoto 606-8203, Japan Laboratorio de Ecologia de Ecossistemas Aquaticos – LEEA, Universidade Federal do Ceara / UFC, Av. Humberto Monte, s/n – PICI, Fortaleza CE, Brazil Laboratorio de Ecologia de Peixes, Departamento de Biologia Geral – ICB, Universidade Federal de Minas Gerais / UFMG, Au. Antonio Carlos, 6627 – Pampulha, Belo Horizonte MG, Brazil Received 11 November 2018; revised 23 March 2019; accepted for publication 28 March 2019 Natural selection often shapes visual perception with respect to the lighting environment. For organisms that rely on visual communication for mating, environmental backscatter and bias in wavelength transmission affect the exchange of visual signals, which can mediate major changes in sexually selected traits. Based on the lighting environment, Amazon forest streams (igarapes) can be categorized into two major water types: clearwater and blackwater. The lighting environment is mostly transparent in clearwater, whereas retention of high amounts of dissolved organic carbon biases light towards the red and creates strong backscatter in blackwater igarapes. We investigated morphological differences among populations representative of lineages within the sailfin tetra Crenuchus spilurus, a sexually dichromatic Amazonian fish. We show that despite the broad geographical range of the nominal species, populations are similar for most measured morphological traits. However, eye diameter and characteristics of the fin ornaments revealed two distinct groups, corresponding to lineages from blackwater and clearwater igarapes. Our results lend support to the sensory drive hypothesis by suggesting that as a consequence of animals inhabiting different lighting conditions, natural selection affected visual perception and thus resulted in differences in sexual ornaments. ADDITIONAL KEYWORDS: divergent selection – lighting environment – morphometrics – visual signals. INTRODUCTION tune to characteristics of the environment (Endler, Sensory systems represent a gateway between 1993a; Endler & Basolo, 1998; Cummings & Partridge, the organism and the environment, transmitting 2001). This process has great potential to generate information vital to the survival of individuals, such biodiversity because senses, preferences and signals as the position of food and potential predators. The can drive divergence among populations when local efficiency of sensory systems depends not only on conditions differ (Servedio & Boughman, 2017). the neural system, but also on the characteristics The biased transmission of specific wavelengths of the medium in which signal transmission occurs and the amount of backscatter often drive evolution (Endler, 1993a; Endler & Basolo, 1998). Thus, natural of light peak sensitivity and the visual perception selection often shapes sensory systems to optimally of organisms (Bowmaker, 1990; Bowmaker & Hunt, 2006; Van Nynatten et al., 2015). Indeed, fine-tuning between environmental colour prevalence and visual Corresponding author. E-mail: [email protected] colour peak sensitivity has been reported for several @ 2019 The Linnean Society of London, Biological Journal of the Linnean Society, 2019, 127, 351-360 351 352 T. H. S. PIRES ET AL. organisms across many different environments ranging from 590 to 700 nm) (Muntz, 1982; Ikeda & (Cummings & Partridge, 2001; Fuller et al., 2003, 2004; Kohshima, 2009). This contrasts with igarapes in Van Nynatten et al., 2015; Cummings & Endler, 2018). clearwater basins, which carry a lesser amount of DOC Because sexual selection results from intraspecific (Mendonca et al., 2005), forming a mostly transparent communication, natural selection shaping the environment without a clear bias in wavelength perception of the environment can pleiotropically transmission (Muntz, 1978, 1982). affect sexually selected traits (Kirkpatrick & Ryan, Differences in water chemistry have increasingly 1991). This effect of natural selection reverberating been highlighted as an important component in on characteristics shaped by sexual selection is the formation of aquatic diversity in the Amazon summarized in the sensory drive hypothesis, which (Beheregaray et al., 2015; Pires et al., 2018). However, poses that signals (typically of males) are a target of the importance of different lighting environments as selection from the sensorial system of communicating a source of diversification remains largely overlooked. individuals (usually females). Because natural Here, we investigate morphological differences selection shapes the sensorial system according to the among populations representative of lineages of environment, it can also lead to changes in sexually the sailfin tetra, Crenuchus spilurus Gunther 1863 selected traits (Endler, 1991; Fuller & Noa, 2010). (Characiformes: Crenuchidae). This nominal species The sensory drive hypothesis also proposes that has a geographical range of over three million square the direction of change is predictable: to increase kilometres that includes the Amazon and Orinoco conspicuousness, the colour of sexually selected traits basins (Pires et al., 2016). Despite its immense should match the prevailing ambient light (Endler, geographical range, the sailfin tetra occurs almost 1992). Sensory drive can promote diversification exclusively in igarapes of black and clear waters. Male and possibly lead to speciation (Boughman, 2002), C. spilurus possess hypertrophied dorsal and anal as suggested for several taxa (Marchetti, 1993; Leal fins that are ornamented in yellow and red (Fig. 1). & Fleishman, 2002; Seehausen et al., 2008; Servedio The presence of such ornaments strongly suggests & Boughman, 2017). Because the combined effects sexual selection based on visual signalling. A previous of sexual and natural selection might cause more study revealed that the nominal species is composed divergence than either alone (Ritchie, 2007; Rundle of two main lineages (i.e. populations with a shared et al., 2009; Kraaijeveldet al., 2011; Maan & Seehausen, common ancestor, Dynesius & Jansson, 2014) that 2011; Network, 2012; Safran et al., 2013), testing the are reproductively isolated. One lineage is composed sensory drive hypothesis represents an important of populations that live in igarapes of the largest step in understanding the generation of biodiversity blackwater river of the Amazon, the Rio Negro (Rio (Servedio & Boughman, 2017). Negro lineage), and a second that occurs throughout With estimates of c. 3000 recognized species and the remainder of the species’ range (Amazonas nearly 100 being newly described every year (Ota lineage) (Pires et al., 2018). These two main lineages et al., 2015), the Amazon is home to the richest can be further divided into sub-lineages, two within freshwater fish fauna on Earth. As described the Rio Negro lineage and at least four sub-lineages of originally by Wallace (1853), Amazon rivers are the Amazonas lineage (Fig. 1).

DISCUSSION in large individuals. Fishes of the two lineages are very similar in eye diameter during the early stages The starkest differences between individuals of development (smaller sizes), but the differences of the Crenuchus spilurus lineages that occupy between individuals of the two lineages become more different lighting environments were observed apparent as individuals grow (Fig. 2D), as expected for morphological characters that reflect visual when comparing closely related organisms (Holtmeier, perception and visual communication, namely eye 2001). diameter, shape and reflectance of ornaments in the Environments with constant dim light often favour dorsal fin, and patterning of ornaments in the anal fin. the evolution of large eyes (Fernald, 1988). Larger lenses are positioned farther away from the retina, increasing the focal length and allowing the excitement of more photoreceptors, which lead to an increased image size on the retina and thus higher visual acuity (the ability to distinguish fine details of objects, especially at long distances) (Collin & Pettigrew, 1989; Bozzano et al., 2001; Parker et al., 2017). As such, differences in eye size between lineages of C. spilurus may stem from ce (%) differences in lighting environment of Amazon forest 600 650 streams (igarapes), the habitat they live in. Blackwater 60 0 igarapes are rich in DOC (Mendonca et al., 2005), Refle which absorbs short wavelengths of light, resulting in a less transparent and red-biased environment when compared to clearwater igarapes. Information on the density of photoreceptors and gan the location of areas of higher cell density on the retina (retinal topography) and differences in opsin genes are 500 Wavelength (nm) 600 650 needed to precisely quantify differences in the visual capabilities of the two sailfin tetra lineages (Douglas & Hawryshyn, 1990; Van Nynatten et al., 2015; Parker Figure 4. Reflectance of the red area of ornaments on et al., 2017). Additionally, studies exploring how the (A) dorsal fin (Rsa region in Fig. 2), and (B) anal fin (Rra differences in visual perception affect behaviour region in Fig. 2). Lines represent individuals, and colours can shed important light on the non-independent represent sub-lineages according to Figure 1. evolution between nsorial system and behaviour, an 2019 The Linnean Society of London, Biological Journal of the Linnean Society, 2019, 127, 351-360 EVOLUTION IN AMAZONIAN LIGHTING ENVIRONMENTS 357 interesting aspect of the sensory drive hypothesis not Although the classification of Amazon freshwater addressed in the present study. environments according to water colour dates to The importance of the lighting environment in early observations of Alfred Russel Wallace (Wallace, sexually selected visual traits has been demonstrated 1853) and despite previous suggestions regarding the for several organisms in a great diversity of importance of the ligh nment in shaping environments (Fuller, 2002; Gomez & Thery, 2004; traits of aquatic organisms in the Amazon (Muntz, Seehausen et al., 2008; Cummings & Endler, 2018). 1982; Ikeda & Kohshima, 2009), this stu When the quality of signal transmission determines of our knowledge, the first to point out the relevance the relative reproductive success of individuals, of Amazon underwater lighting environment in sexual selection operates and changes the frequencies generating biodiversity relative to other evolutionary of signal-transmission traits (Andersson, 1994; forces (genetic drift and other potential selection Endler & Houde, 1995). Notoriously, the presence of pressures on morphological traits). Logistic difficulties large amounts of DOC in water has been previously of sampling and transporting live organisms in a addressed and shown to modulate female choice in mostly pristine forest environment probably deterred guppies (Endler & Houde, 1995). previous investigations. By comparing closely related Characteristics of the colour pattern and reflectance organisms (lineages within the nominal C. spilurus), of the dorsal fin in Rio Negro lineage individuals we showed that evolution of secondary sexual traits differ from those observed among Amazonas lineage outpaced changes occurring in other measured traits. individuals. Red and black stripes on the dorsal The sailfin tetra is one of few fish species that occurs in fin are typically larger and broader in individuals igarapes from basins of distinct water types, and that of the Rio Negro lineage. Such large area of red show strong sexual dimorphism and dichromatism stripe apparently contributes to the observed higher (Pires et al., 2016). As such, the sailfin tetra provides reflectance of longer wavelengths, red pigments a clear opportunity to study the effects of different accumulate in a gradient along the stripe. The higher underwater lighting environments in generating expression of the most abundant wavelengths in an biodiversity. environment increases brightness (Endler, 1993b; Differences in water characteristics mediating McDonald et al., 1995), which, together with the higher biological diversification in the Amazon have expression of black, suggests increased contrast and increasingly been reported (Cooke et al., 2012, 2014; conspicuousness of the dorsal fin of Rio Negro males Beheregaray et al., 2015). Such studies have focused on under red-biased lighting. The shape of the dorsal fin the role of water chemistry in speciation, e pecially the is also different between the Rio Negro and Amazonas differences in relation to pH and conductivity across lineages. Live individuals of the Rio Negro linea water types (Cooke et al., 2012, 2014; Beheregaray a flame-shaped dorsal fin (Fig. 3, lower inset) whereas et al., 2015). For C. spilurus, Pires et al. (2018) the upper outline of the dorsal fin of individuals of the suggested that reproductive isolation between the two Amazonas lineages is more evenly distributed (Fig. 3, main lineages of C. spilurus is mediated by differences upper inset). This difference in dorsal fin shape is in osmoregulation. However, their study controlled for mostly driven by different positioning of landmarks water colour and thus did not consider the importance 6-9, which represent positions of the most posterior of lighting environments in mediating reproductive dorsal fin rays. Importantly, the last five rays of the isolation. Because rough colour dorsal fin are used by the fish for fine movements when signals may play an important role in mate choice swimming (Pires et al., 2016). Therefore, differences and speciation (Endler & Houde, 1995; Seehausen & in such rays can also have consequences for natural Van Alphen, 1998; Boughman, 2001; Caro, 2018), our selection. Overly small or large rays can impair study raises the interesting possibility that differences manoeuvrability, swimming capacity or efficiency of in lighting condition may also contribute to the signal transmission by ornaments of the dorsal fin. It evolution of reproductive isolation between lineages of seems promising for future studies to explore whether C. spilurus. the differences reported here reflect different points Although the sensory drive hypothesis highlights of the balance between natural selection favouring sexual selection from female choice, the importance of swimming abilities and sexual selection favouring male-male competition in the evolution of ornaments signal transmission. Colour patterning of the a is largely underexplored (Berglund et al., 1996; also differed between lineages, with individuals of the Candolin & Tukiainen, 2015) and seems to play a very Rio Negro lineage showing larger and less numerous important role in interactions among individuals of spots, whereas the opposite trend was observed for C. spilurus. Because male traits might lead to successful individuals of the Amazonas lineage, evidenceng reproduction, which may depend on the habitat in which further differences in signal transmission between competition and mating occur (Lackey & Boughman, lineages 2013), empirical evidence is needed to assess whether @ 2019 The Linnean Society of London, Biological Journal of the Linnean Society, 2019, 127, 351-360 358 T. H. S. PIRES ET AL. male-male competition or female mate choice plays Andersson MB. 1994. Sexual selection. Princeton: Princeton a major role in the evolution of sexually selected University Press. characters in C. spilurus. Moreover, the mechanisms Arnegard ME, Mcintyre PB, Harmon LJ, Zelditch ML, of sexual selection might affect different aspects of the Crampton WG, Davis JK, Sullivan JP, Lavoue S ornaments. For instance, because the ornaments in the Hopkins CD. 2010. Sexual signal evolution outpaces anal fin are only displayed during interactions between ecological divergence during electric fish species radiation. two individuals, they might play a central role in mate The American Naturalist 176: 335-356. choice. On the other hand, because the dorsal fin is Arnott G, Elwood RW. 2009. Asses sment of fighting ability in displayed during regular swimming movements, it can animal contests. Animal Behaviour 77: 991-1004. broadcast information on dominance status. Beheregaray LB, Cooke GM, Chao NL, Landguth EL. 2015. Many non-ornament traits (e.g. body length Ecological speciation in the tropics: insights from comparative and height) are typically important in male-male genetic studies in Amazo ntiers in Genetics 5: 1-19. competition. However, such traits might be constrained Berglund A, Bisazza A, Pilastro A. 1996. Armaments and to evolve due to correlation with other traits. For ments: an evolutionary explanation of traits of dual utility. Biological Journal of the Linnean Society 58: 385-399. instance, while body size is the most important feature Boughman JW. 2001. Divergent sexual selection enhances in determining the outcome of contests between males reproductive isolat (Briffa, 2008; Arnott & Elwood, 2009), changes in Boughman JW. 2002. How sensory drive can promote maximum body size are often coupled with delayed speciation. Trends in Ecology and Evolution 17: 571-577. age at first maturity (Roff, 1992), which can result in Bowmaker JK. 1990. Visual pigments of fishes. In: Douglas R, a potential decrease in lifetime fitness. Ornaments, on Djamgoz M, eds. The visual system of fish. London: Chapman the other hand, represent a direct result of selection and Hall, 81-107. stemming from communication among conspecifics, Bowmaker JK, Hunt DM. 2006. Evolution of vertebrate and are thus not strongly constrained by correlation visual pigments. Current Biology 16: R484-R489. with other traits. ozzano A, Murgia R, Vallerga S, Hirano J. Archer S. The results reported here align with the sensory 2001. The photoreceptor system in the retinae of two drive hypothesis (Endler, 1992; Boughman, 2002), dogfishes, Scyliorhinus canicula and Galeus melastomus: which poses that sensorial systems evolve by tuning to possible relationship with depth distribution and predatory local environmental conditions where communication lifestyle. Journal of Fish Biology 59: 1258-1278. occurs, in turn affecting the evolution of sexually Briffa M. 2008. Decisions during fights in the house cricket, selected characters (Servedio & Boughman, 2017). Acheta domesticus: mutual or self assessment of energy, Specifically, the distinct light transmission between weapons and size? Animal Behaviour 75: 1053-1062. different coloured igarapes could have affected visual Candolin U, Tukiainen I. 2015. The sexual selection traits of C. spilurus, with subsequent sexual selection paradigm: have we overlooked other mechanisms in the shaping the evolution of the ornaments. evolution of male ornaments? Proceedings of the Royal Society B: Biological Sciences 282: 20151987.

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