It has been 25 years since the formalization of the Sensory Drive hypothesis was published in the American Naturalist (1992). Since then, there has been an explosion of research identifying its util- ity in contributing to our understanding of inter- and intra-speciﬁc variation in sensory systems and signaling properties. The main tenet of Sensory Drive is that environmental characteristics will inﬂuence the evolutionary trajectory of both sensory (detecting capabilities) and signaling (detect- able features and behaviors) traits in predictable directions. We review the accumulating evidence in 154 studies addressing these questions and categorized their approach in terms of testing for environmental inﬂuence on sensory tuning, signal characteristics, or both. For the subset of studies that examined sensory tuning, there was greater support for Sensory Drive processes shaping vis- ual than auditory tuning, and it was more prevalent in aquatic than terrestrial habitats. Terrestrial habitats and visual traits were the prevalent habitat and sensory modality in the 104 studies show- ing support for environmental inﬂuence on signaling properties. An additional 19 studies that found no supporting evidence for environmental inﬂuence on signaling traits were all based in ter- restrial ecosystems and almost exclusively involved auditory signals. Only 29 studies examined the complete coevolutionary process between sensory and signaling traits and were dominated by ﬁsh visual communication. We discuss biophysical factors that may contribute to the visual and aquatic bias for Sensory Drive evidence, as well as biotic factors that may contribute to the lack of Sensory Drive processes in terrestrial acoustic signaling systems. Key words: animal communication, sensory drive, sensory ecology, sexual selection The Origins of Sensory Drive models was to explain how male signaling traits could become com- When reviewing the evidence or impact of a particular scientific hy- mon within a population. Meanwhile, there was little scientific dis- pothesis, it is useful to provide the historical context in which it origi- cussion put forth for proposing models to predict which traits, or the nated. At the time of the late 1980s, there were three main models for specific features of male traits, that would be selected for under sexual the evolution of female mate choice and the traits that males evolve to selection, nor was there much interest in the effects of the signalling secure matings; Fisher’s runaway, Direct benefits, and Indirect bene- environment and sensory processes. fits (good genes). For all three of these, the specific features of the At the same time that sexual selection models in the 1980s were male signal evolved to either genetically run away with female choice largely blind to sensory inputs, the field of sensory ecology was al- genes, indicate direct benefits to females, or indicate indirect benefits ready well established and fully focused on how signaling traits and to offspring, and the direction of evolution was assumed to be arbi- sensory systems are shaped by environments. Interest in the diversity trary (Bradbury et al.,1987). At the time, the purpose of all of these of birdsong led researchers to test whether differential transmission V C The Author(s) (2018). Published by Oxford University Press. 471 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/64/4/471/5034003 by Ed 'DeepDyve' Gillespie user on 22 August 2018 472 Current Zoology, 2018, Vol. 64, No. 4 properties of species’ habitats was at the source of this variation (“the environmental selection hypothesis” Morton 1975; Richards and Wiley 1980). Similarly, visual ecology pioneers such as John Lythgoe, William McFarland, and others were taking a highly quan- titative approach to determine whether visual pigments covaried with different underwater optical environments (McFarland and Munz 1975; Lythgoe 1979). Given the highly predictive power of sensory ecology coupled with the absence of predictive sexual selec- tion models at this time, it is perhaps not surprising that a number of “sensory-”based models for female mate choice/male signaling trait evolution emerged on the scene in the early 1990s. Endler pre- sented Sensory Drive in a discussion during the Dahlem Conference on Sexual Selection in 1987 and a follow-up symposium (Endler 1992a) from which the first formal description of Sensory Drive emerged (Endler 1992b). The idea spread and features of this model were explored in more detail by several people. Among these were Sensory Exploitation (Ryan and Rand 1990); Pre-existing Bias (Basolo 1990, 1995) and Sensory Traps (Christy 1995). All of these “sensory” models can be placed in the Sensory Drive scheme (see Endler and Basolo 1998 for a comparative review of these models), but for the purposes of this review we will restrict our focus to describing and accumulating evidence for the overall Sensory Drive model (Figure 1). While all sensory or receiver bias models contend that male signal evolution is predicted by female sensory biases, only the Sensory Drive model (described in detail below) explicitly Figure 1. The Sensory Drive Model (modiﬁed from Endler 1992b). Steps describes from where those sensory biases arise and include the coded in green represent the sensory component of the Sensory Drive model effects of the environment on both the signaller and senses (Endler as the environment places selective forces on the evolution of sensory sys- 1992b; Endler and Basolo 1998). tem properties for food detection but that also inﬂuences female mate choice criteria. Steps of the model that incorporate sensory exploitation are indi- cated by asteriesk. Steps colored in blue represent the signalling component of the Sensory Drive model describing the evolution of signaling characteris- What is Sensory Drive? tics (ornament features, behavioral displays, and choice of microhabitat for The Sensory Drive model outlined by Endler (1992b, 1993) was a display) that are predictable products of environmental constraints and/or truly comprehensive and predictive model for the origins of commu- responses to environmentally shaped female response biases. Note that the environment is featured in both components (sensory and signal tuning), nication traits. In this model, both signal receiver preference func- hence that box is bi-colored. Except for those arrows with text, the arrows tions and signal transmitter traits are predictable characters based indicate evolutionary relationships. The combined effects of microhabitat on features of a species’ environment. The two main components of choice and behaviour have immediate effects on the signalling environment. a communication dyad (receiver behavior and signaling traits) both Neural crest cells affect colour patterns directly but are developmentally co-evolve under the constraints of the abiotic (physical) and biotic related to other cells in the neural system. This is a new component of (predatory and foraging) environment. While this model built upon Sensory Drive. previous sensory ecology insights into how the environment is likely stimulation); this portion of Sensory Drive is known as Sensory to shape sensory systems and imposes constraints on signal transmis- Exploitation (Endler 1992b; Endler and Basolo 1998). sion properties, it broadened the model to include how these envir- Part of the difficulty in reviewing the presence or absence of sup- onmental features influence key behaviors involved in the sexual port for Sensory Drive is clarifying which portion of the Sensory Drive selection process (mate choice and display behavior) and put it to- model is under examination; and/or whether researchers are able to gether in a larger evolutionary model. To quote directly from Endler test Sensory Drive in its entirety. There are many interacting steps (1992b), “These suites of traits should coevolve in predictable direc- involved in Sensory Drive (Figure 1) and researchers have taken a tions, determined by environmental biophysics, neurobiology and number of different approaches or have emphasized different subsets the genetics of the suites of traits- hence the term ‘sensory drive’.” of steps in the model. To organize our discussion we divide Sensory The critical feature that encapsulates the Sensory Drive hypoth- Drive into two components, sensory and signalling. The sensory com- esis is the environment. As shown in Figure 1 (modified from Endler ponent of the Sensory Drive model predicts a tight correlation between 1992b), the environmental conditions during communication events receiver sensory detection properties and features within a species’ place selective pressures on the sensory systems to detect important physical environment outside the realm of reproduction. The other features in its specific habitat (foraging items or other important major component of the Sensory Drive model, the signaling compo- traits under natural selection) and this influences receiver responses nent, relates to the evolution of signaling traits in the communication during mate choice encounters. Receivers with a sensory bias shaped dyad. It focuses on the strength of environmental constraints in shap- by the biophysical properties of their habitat are likely to detect ing signal evolution to both match environmentally-induced sensory some stimuli better than others. This detection bias will result in biases of the signal receiver and environmental transmission or other receiver biases during mate choice and other choice encounters. habitat features. Here, we present the evidence that has accumulated For example, males that have communication features that match over 25 years in more detail, and examine some of the patterns that a female’s detectability bias will enjoy a detectability advantage are emerging across habitats, modalities, and taxa. (seen, heard, smelled or felt first and/or with the greatest sensory Downloaded from https://academic.oup.com/cz/article-abstract/64/4/471/5034003 by Ed 'DeepDyve' Gillespie user on 22 August 2018 Cummings and Endler. Sensory drive evidence and its watery bias 473 Evidence for Sensory Drive steps in Figure 1). These studies found overwhelming support for the sensory component of the sensory drive model with 53 studies iden- Since the early 1990s, much work has examined whether environmen- tifying support of sensory drive while 3 did not. Researchers inter- tal variation can predict variation in the coevolution of sensory sys- ested in testing this component of the Sensory Drive hypothesis have tems and signal design. Recent reviews of the model have found much often compared biophysical measurements from species-specific empirical support for Sensory Drive processes (Cole 2013; Ryan and habitats with physiological measurements of sensory perception Cummings 2013; Price 2017), as well as some studies finding little evi- (e.g., Cummings and Partridge 2001; Cheroske et al. 2003; Fuller dence for its role in signal differentiation (Ey and Fischer 2009; et al. 2003, 2004; Cummings 2004, 2007; Carleton et al. 2005; Malone et al. 2014). In our review, we decided to examine the evi- Seehausen et al. 2008; Fuller and Noa 2010; Veilleux et al. 2013; dence for Sensory Drive in its most classic form — with an emphasis Veilleux and Cummings 2012; Bloch 2015; Bloch et al. 2015a; on environmental influence. Hence, we have limited our review to Sandkam et al. 2015; Tuset et al. 2016). Yet, in order to determine studies that examine whether environmental variation can predict if this detectability bias has pleiotropic effects spilling into the sexual variation in sensory tuning, signal characteristics or both. This means selection domain requires determining if these biases play a role in that several excellent studies that study Sensory Exploitation/Pre- mate choice decisions. A few researchers have comprehensively existing Bias without an environmental component are not included tested this logistically complex question (e.g., Boughman 2001; in this current review (e.g., Basolo 1990; Ryan and Rand 1990; Rodd et al. 2002; Garcia and Ramirez 2005; Maan et al. 2006; Rosenthal and Evans 1998; and others reviewed in Ryan and Seehausen et al. 2008; Arnqvist and Kolm 2010). Cummings 2013). This exclusion is not meant to diminish the import- Of the studies that found evidence for sensory drive processes ance of Sensory Exploitation sensu strictu (the binding glue between influencing sensory system tuning, 57% were in aquatic environ- sensory and signal coevolution) but rather focus our review around ments (Figure 2) and 83% involved vision (Figure 3). These studies the feature that sets this coevolutionary process in motion (according were also dominated by teleost fish (45%) followed by invertebrates to Sensory Drive) — the environment. It also allows us to ask ques- (19%), birds (15%), mammals (9%), and reptiles (8%, Figure 4). tions about habitat bias in Sensory Drive studies, and whether some Using a Freeman–Halton exact test to compare the evidence for and habitats show more support for Sensory Drive processes than others. against the sensory component of sensory drive, we found no signifi- We also ask whether certain components in the Sensory Drive model cant differences in habitat, modality, or taxonomic group (Table 2). are better supported than others; and whether the support for Sensory However, given so few studies in the “no evidence” column, a statis- Drive is biased for specific sensory modalities or taxonomic groups. tical approach to identify patterns is anemic from the beginning. To examine the evidence for Sensory Drive and probe for habi- Nonetheless, it is worth noting that the vast majority of these sen- tat, modality, and taxonomic bias, we conducted a literature review sory studies fell in the domain of vision. Is this because human of empirical studies in the field. For habitat classification, we catego- researchers are visually biased? Or is it because visual tuning is an rized organisms communicating in either terrestrial or aquatic (both easier modality to test in the lab and field? Or does vision marine and freshwater) ecosystems. We searched for taxonomic bias respond more to the optical environment than the auditory senses to by comparing the evidence for and against Sensory Drive between the auditory environment? Patterns could be entirely different in invertebrates and the major vertebrate classes; there were insuffi- other sensory modes, for which there are still few data. cient invertebrate studies to subdivide them by taxa. We restricted our analysis to the two most commonly investigated sensory modal- Environmental tuning mechanisms favor vision over ities — vision and audition (with a modicum of vibration) due to the other modalities? relative paucity of studies in other modes such as electroreception Is there a mechanistic advantage of vision to respond to the environ- and chemoreception. While tests of Sensory Drive within chemo- ment more than the other sensory modalities? Vision scientists have reception are beginning to accumulate (see references within Cole been able to document how responsive the visual pathway is to 2013), they are both few and relatively recent and we encourage fu- environmental inputs in a number of taxa. Since the 1960s, it has ture reviews to probe for habitat or taxonomic biases for chemosen- been well documented that many teleosts employ a mixed chromo- sory Sensory Drive processes. phore strategy (different proportions of A1 and A2 prosthetic Overall, we identified 154 studies that examined the evidence for groups in photoreceptor outer segments) to tune their spectral sensi- some (or most) steps in the sensory drive model. Of these studies, tivity to ambient light conditions (Dartnall et al. 1961; Bridges 132 (86%) found evidence for Sensory Drive and 22 (14%) did not 1965, 1972; Munz and Beatty 1965; Allen 1971; Loew and Dartnall (Tables 1 and 2). While we should expect some portion of this lop- 1976; Levine and MacNichol 1979; Muntz and Mouat 1984). More sided ledger to be driven by a reporting bias for positive results, our recent work has also shown how differential expression of multiple aim with this review is to identify any patterns that are emerging in opsin proteins in photoreceptor outer segments is biased based on terms of where, in what sensory modality, and with what organism optical inputs during development (Carleton and Kocher 2001; do we see greater or lesser support for the sensory drive model. Fuller et al. 2004; Shand et al. 2008; Hofmann et al. 2010) as well We examine the evidence for and against sensory drive in each of as dietary influences (Sandkam et al. 2016). And we have become the main components of sensory drive (sensory and signaling) separ- even more aware that sensory tuning can shift across the course of ately as well as the model as a whole. For each of these examina- a day (Johnson et al. 2013); or as a function of steroid hormonal tions, we then compare the evidence in terms of habitat, modality exposure (e.g., Friesen et al. 2017). and taxonomic support. Note that many of these visual “tuning” mechanisms are restricted to certain aquatic taxa. Some fish and amphibian species Evidence for the environment influencing sensory contain dual chromophores in their retina (A1 and A2). By changing components the ratio of A1:A2 in each photoreceptor’s outersegment, these We identified 56 empirical studies (Table 1) that directly tested the aquatic and semi-aquatic species can tune the absorption maxima of sensory component predictions of the sensory drive model (green the photoreceptor to match properties of their ambient light Downloaded from https://academic.oup.com/cz/article-abstract/64/4/471/5034003 by Ed 'DeepDyve' Gillespie user on 22 August 2018 474 Current Zoology, 2018, Vol. 64, No. 4 Table 1. Characterization of 154 studies evaluating sensory drive processes by taxonomic grouping, sensory modality, habitat, and whether they demonstrated support for the sensory, signaling components of the sensory drive model. Major taxonomic Species group Sense Habitat Sensory Signal Citation group support support Invertebrates Beetle Vision Terrestrial Yes Yes The ´ ry et al. (2008) Invertebrates Bladder grasshoppers Auditory Terrestrial Yes Couldridge and van Staaden (2004) Invertebrates Butterﬂies Vision Terrestrial Yes Rutkowski et al. (2007) Invertebrates Cicadas Auditory Terrestrial No Sueur and Aubin (2003) Invertebrates Crabs Vision Terrestrial Yes Christy (1988) Invertebrates Crabs Vision Terrestrial Yes Yes Christy (1995) Invertebrates Crabs Vision Terrestrial Yes Christy et al. (2002) Invertebrates Crabs Vision Terrestrial Yes Yes Christy et al. (2003) Invertebrates Crabs Vision Terrestrial Kim et al. (2007) Invertebrates Crickets Auditory Terrestrial No Forrest (1991) Invertebrates Crickets Auditory Terrestrial No Jain and Balakrishnan (2012) Invertebrates Crickets Auditory Terrestrial No Mendelson and Shaw (2005) Invertebrates Green Lacewings Auditory Terrestrial No Noh and Henry (2010) Invertebrates Green Lacewings Auditory Terrestrial No Henry and Wells (2004) Invertebrates Moths Auditory Terrestrial Yes Conner (1987) Invertebrates Water Mites* Vibratory* Aquatic Yes Yes Proctor (1991) Invertebrates Water Mites* Vibratory* Aquatic Yes Yes Proctor (1992) Invertebrates Spiders Vision Terrestrial Yes Scheffer et al. (1996) Invertebrates Spiders Vision Terrestrial Yes Clark (2011) Invertebrates Spiders Vision Terrestrial Yes Wilgers and Hebets (2011) Invertebrates Spiders* Vibratory* Terrestrial Yes Elias et al. (2010) Invertebrates Stomatopods Vision Aquatic Yes Cronin et al. (2001) Invertebrates Stomatopods Vision Aquatic Yes Cronin and Caldwell (2002) Invertebrates Stomatopods Vision Aquatic Yes Cheroske et al. (2003) Invertebrates Stomatopods Vision Aquatic Yes Cheroske et al. (2006) Invertebrates Treehoppers* Vibratory* Terrestrial Yes Sullivan-Beckers and Cocroft (2010) Invertebrates Treehoppers* Vibratory* Terrestrial Yes McNett and Cocroft (2008) Fish Characins Vision Aquatic Yes Yes Arnqvist and Kolm (2010) Fish Lake Malawi Cichlids Vision Aquatic No Smith et al. (2012) Fish Lake Victoria Cichlids Vision Aquatic Yes Seehausen et al. (1997) Fish Lake Victoria Cichlids Vision Aquatic Yes Yes Maan et al. (2017) Fish Lake Victoria Cichlids Vision Aquatic Yes Carleton et al. (2005) Fish Lake Victoria Cichlids Vision Aquatic Yes Yes Seehausen et al. (2008) Fish Lake Victoria Cichlids Vision Aquatic Yes Yes Maan et al. (2006) Fish Goodeids Vision Aquatic Yes Yes Garcia and Ramirez (2005) Fish Guppies Vision Aquatic Yes Endler (1980) Fish Guppies Vision Aquatic Yes Yes Endler (1983) Fish Guppies Vision Aquatic Yes Endler (1987) Fish Guppies Vision Aquatic Yes Yes Endler (1991) Fish Guppies Vision Aquatic Yes Yes Endler (1995) Fish Guppies Vision Aquatic Yes Cole and Endler (2016) Fish Guppies Vision Aquatic Yes Long and Rosenqvist (1998) Fish Guppies Vision Aquatic Yes Chapman et al. (2009) Fish Guppies Vision Aquatic Yes Yes Rodd et al. (2002) Fish Guppies Vision Aquatic Yes Yes Gamble et al. (2003) Fish Guppies Vision Aquatic Yes Sandkam et al. (2015) Fish Killiﬁsh Vision Aquatic Yes Fuller et al. (2003) Fish Killiﬁsh Vision Aquatic Yes Fuller et al. (2005) Fish Killiﬁsh Vision Aquatic Yes Yes Fuller and Noa (2010) Fish Killiﬁsh Vision Aquatic Yes Fuller (2002) Fish Killiﬁsh Vision Aquatic Yes Fuller and Travis (2004) Fish Ornate Rainbow Fish Vision Aquatic Yes Hancox et al. (2013) Fish Reef ﬁsh Vision Aquatic Yes Yes Marshall (2000) Fish Rockﬁsh Auditory Aquatic Yes Tuset et al. (2016) Fish Southern Pygmy perch Vision Aquatic Yes Morrongiello et al. (2010) Fish Sticklebacks Vision Aquatic Yes Reimchen (1989) Fish Sticklebacks Vision Aquatic Yes Yes Boughman (2001) Fish Sticklebacks Vision Aquatic Yes Yes Smith et al. (2004) Fish Sticklebacks Vision Aquatic Yes Veen et al. (2017) Fish Sticklebacks Vision Aquatic Yes Yes Brock et al. (2017) (continued) Downloaded from https://academic.oup.com/cz/article-abstract/64/4/471/5034003 by Ed 'DeepDyve' Gillespie user on 22 August 2018 Cummings and Endler. Sensory drive evidence and its watery bias 475 Table 1. (continued) Major taxonomic Species group Sense Habitat Sensory Signal Citation group support support Fish Suluwesi Fish Vision Aquatic Yes Gray et al. (2008) Fish Surfperch Vision Aquatic Yes Cummings and Partridge (2001) Fish Surfperch Vision Aquatic Yes Cummings (2004) Fish Surfperch Vision Aquatic Yes Yes Cummings (2007) Amphibians Bolivian frogs Auditory Terrestrial No Bosch and Riva (2004) Amphibians Central Amazon frogs Auditory Terrestrial No Zimmerman (1983) Amphibians Central Amazon frogs Auditory Terrestrial No Kime et al. (2000) Amphibians Chorus frogs Auditory Terrestrial No Malone et al. (2014) Amphibians Concave-eared Torrent frog Auditory Terrestrial Yes Yes Feng et al. (2006) Amphibians Cricket frogs Auditory Terrestrial Yes Ryan et al. (1990) Amphibians Cricket frogs Auditory Terrestrial Yes Gamble et al. (2008) Amphibians Cricket frogs Auditory Terrestrial Yes Witte et al. (2005) Amphibians Green toads Auditory Terrestrial No Castellano et al. (2003) Amphibians Poison Frogs Vision Terrestrial Yes Maan and Cummings (2012) Amphibians Poison Frogs Vision Terrestrial Yes Cummings and Crothers (2013) Amphibians Rock Frogs Vision Terrestrial Yes Grafe et al. (2012) Amphibians Rock skipper frog Auditory Terrestrial Yes Boeckle et al. (2009) Amphibians South American frogs Auditory Terrestrial No Penna and Solis (1998) Amphibians Streambank frogs Auditory Terrestrial Yes Odendaal et al. (1986) Amphibians Thailand frogs Auditory Terrestrial Yes Sun and Narins (2005) Amphibians Toads Auditory Terrestrial Yes Ryan and Sullivan (1989) Amphibians Treefrogs Auditory Terrestrial Yes Ziegler et al. (2011) Amphibians Tree-hole frogs Auditory Terrestrial Yes Lardner and Lakim (2002) Reptiles Anolis lizards Vision Terrestrial Yes Yes Sigmund (1983) Reptiles Anolis lizards Vision Terrestrial Yes Yes Leal and Fleishman (2002) Reptiles Anolis lizards Vision Terrestrial No Steinberg and Leal (2016) Reptiles Anolis lizards Vision Terrestrial Yes Yes Fleishman (1992) Reptiles Anolis lizards Vision Terrestrial Yes Yes Leal and Fleishman (2004) Reptiles Anolis lizards Vision Terrestrial Yes LeBas and Marshall (2000) Reptiles Anolis lizards Vision Terrestrial Yes Ord et al. (2007) Reptiles Anolis lizards Vision Terrestrial Yes Peters and Evans (2003) Reptiles Anolis lizards Vision Terrestrial Yes Peters et al. (2007) Reptiles Chameleons Vision Terrestrial Yes Stuart-Fox et al. (2007) Reptiles Chameleons Vision Terrestrial Yes Stuart-Fox and Moussalli (2008) Birds Amazonian birds Auditory Terrestrial Yes Tobias et al. (2010) Birds American redstarts Auditory Terrestrial No Date and Lemon (1993) Birds Antbirds Auditory Terrestrial Yes Nemeth et al. (2001) Birds Blue tits Auditory Terrestrial No Doutrelant and Lambrechts (2001) Birds Bowerbirds Vision Terrestrial Yes Yes Madden and Tanner (2003) Birds Bowerbirds Vision Terrestrial Yes Yes Endler and Day (2006) Birds Bowerbirds Vision Terrestrial Yes Doucet and Montgomerie (2003) Birds Bowerbirds Vision Terrestrial Yes Endler et al. (2010) Birds Bowerbirds Vision Terrestrial Yes Kelley and Endler (2012) Birds Bowerbirds Vision Terrestrial No Borgia and Keagy (2006) Birds Carolina Wren Auditory Terrestrial Yes Gish and Morton (1981) Birds Chickens Vision Terrestrial Yes Hart et al. (2006) Birds Finches Auditory Terrestrial Yes Snell-Rood and Badyaev (2008) Birds Finches Auditory Terrestrial No Podos (2010) Birds Flycatchers Auditory Terrestrial Yes Francis et al. (2011) Birds Forest Birds Auditory Terrestrial Yes Ryan and Brenowitz (1985) Birds Forest Birds Vision Terrestrial Yes Endler and The ´ ry (1996) Birds Forest Birds Vision Terrestrial Yes Gomez and The ´ ry (2004) Birds Forest Birds Vision Terrestrial Yes Gomez and The ´ ry, 2007. Birds Forest Birds Vision Terrestrial Yes Uy and Stein (2007) Birds Great tits Auditory Terrestrial Yes Yes Mockford and Marshall (2009) Birds Great tits Auditory Terrestrial Yes Slabbekoorn and Peet (2003) Birds Great tits Auditory Terrestrial Yes Slabbekoorn and der Boer-Vissor (2006) Birds Green hylia Auditory Terrestrial Yes Kirschel et al. (2009) Birds Grey breasted wood wren Auditory Terrestrial Yes Dingle et al. (2008) Birds House ﬁnches Auditory Terrestrial Yes Bermudez-Cuamatzin et al. (2011) Birds Juncos Auditory Terrestrial Yes Slabbekoorn et al. (2007) (continued) Downloaded from https://academic.oup.com/cz/article-abstract/64/4/471/5034003 by Ed 'DeepDyve' Gillespie user on 22 August 2018 476 Current Zoology, 2018, Vol. 64, No. 4 Table 1. (continued) Major taxonomic Species group Sense Habitat Sensory Signal Citation group support support Birds Mannakins Vision Terrestrial Yes Uy and Endler (2004) Birds Mannakins Vision Terrestrial Yes Heindl and Winkler (2003) Birds Nightingales Auditory Terrestrial Yes Brumm (2004) Birds Nightingales Auditory Terrestrial Yes Sorjonen (1986) Birds North American oscines Auditory Terrestrial Yes Wiley (1991) Birds Robins Auditory Terrestrial Yes Fuller et al. (2007) Birds Silvereyes Auditory Terrestrial Yes Potvin et al. (2011) Birds Song Sparrows Auditory Terrestrial Yes Shy and Morton (1986) Birds Song Sparrows Auditory Terrestrial Yes Patten et al. (2004) Birds South African birds Auditory Terrestrial No Saunders and Slotow (2004) Birds Warblers Vision Terrestrial Yes Marchetti (1993) Birds Warblers Auditory Terrestrial No Fotheringham et al. (1997) Birds Warblers Vision Terrestrial Yes Bloch (2015) Birds Warblers Vision Terrestrial Yes Bloch et al. (2015a) Birds Warblers Vision Terrestrial Yes Bloch et al. (2015b) Birds Warblers Vision Terrestrial Yes Price (2017) Birds White Crown Sparrows Auditory Terrestrial Yes Derryberry (2009) Mammals Baboons Auditory Terrestrial Yes Ey et al. (2009) Mammals Bats Auditory Terrestrial Yes Arlettaz et al. (2001) Mammals Bats Auditory Terrestrial Yes Jacobs et al. (2017) Mammals Bats Auditory Terrestrial No Puechmaille et al. (2011) Mammals Japanese macaques Auditory Terrestrial Yes Sugiura et al. (2006) Mammals Lemurs Vision Terrestrial Yes Veilleux et al. (2013) Mammals Marmots Auditory Terrestrial Yes de la Torre and Snowdon (2002) Mammals Marmots Auditory Terrestrial Yes Daniel and Blumstein (1998) Mammals New World Monkeys Auditory Terrestrial Yes Brumm et al. (2003) Mammals Nocturnal mammals Vision Terrestrial Yes Veilleux and Cummings (2012) Mammals Primates Vision Terrestrial Yes Fernandez and Morris (2007) Mammals Primates Auditory Terrestrial Yes Waser and Waser (1977) Mammals Primates Auditory Terrestrial Yes Mitani and Stuht (1998) Mammals Rain forest monkeys Auditory Terrestrial Yes Brown et al. (1995) Mammals Savannah monkeys Auditory Terrestrial No Brown et al. (1995) Mammals Whales Auditory Aquatic Yes Miller et al. (2000) Asterisk refers to examples of sensory drive that involve the vibratory sensory system (included in this table, but not included for statistical analyses in table 2 owing to small numbers). conditions. Evidence for chromophore mixing to match spectral variation has been attributed to variation in foraging ecology (Hart properties of the underwater environment has been found in fresh- 2001). Furthermore, many birds and reptiles contain pigmented oil water (Bridges 1972; Loew and Dartnall 1976), saltwater droplets in the inner segments of their photoreceptors that reduce (Cummings and Partridge 2001) and anadromous fish (Munz and the intensity and narrow the spectrum of light impinging upon the Beatty 1965; Muntz and Mouat 1984). Furthermore, teleosts have visual pigment in the outer segment (Liebman and Granda 1971; shown greater plasticity than any other taxon in spectral tuning via Bowmaker 1977; Loew et al. 2002); and the amount of this inner differential expression in opsin proteins within their photoreceptors segment colored pigment appears to vary by ambient light intensity (Fuller et al. 2004, 2010; Hofmann et al. 2009, 2010; Carleton (Hart et al. 2006). 2009; Parry et al. 2005). Moreover, marine invertebrates, such as Interestingly, there is robust evidence of olfactory systems being stomatopods, have multiple means to alter spectral sensitivity via tuned to their physical environment. Since early work in the 1970s modification to intrarhabdomal filters, allowing for extensive tuna- (Scholz et al. 1976), we have seen that the fish olfactory epithelium bility (Cronin et al. 2001; Marshall et al. 2007). responds to sensory input by a positive feedback process that allows While terrestrial vertebrates (amphibians, reptiles, birds, and salmon to tune their olfactory pathway to detect the olfactory signa- mammals) do not possess as many tuning mechanisms as some of tures of their specific birth tributary (Harden et al. 2006). The olfac- the marine organisms [e.g., only a single chromophore (A1)], they tory system may well be set up to be primed by early developmental still exhibit tunable variation in visual sensitivities. Warblers exhibit conditions to recognize certain odors for later olfactory discrimin- differential opsin expression between species that vary in optical ation (e.g., kin selection, Hinz et al. 2013). In fact, this phenomenon habitats (Bloch 2015), as well as genetic variation in opsin genes may occur in a variety of taxa, including insects at various develop- that is functionally linked to changes in habitat use (Bloch et al. mental stages (Davis and Stamps 2004). 2015a). Birds, in general, exhibit tremendous genetic variation in What is the evidence for sensory tuning to the acoustic environ- UV-sensitive cone opsins (SWS1, Hart and Hunt 2007), and vari- ment? It is clear that the auditory systems from invertebrates ation in the proportion of different photoreceptor cone types. This (Schmidt et al. 2011) to vertebrates (Witte et al. 2005; Bar-Yosef Downloaded from https://academic.oup.com/cz/article-abstract/64/4/471/5034003 by Ed 'DeepDyve' Gillespie user on 22 August 2018 Cummings and Endler. Sensory drive evidence and its watery bias 477 Table 2. Results of freeman-halton exact test results comparing dif- ferences in habitat, modality, and taxonomic group characteristics of supporting (yes) and non-supporting (no) studies testing the sensory (A), signaling (B), or both components (C) of the sensory drive model A. Number studies testing the ﬁrst component of Sensory Drive (Sensory systems tuned to environmental parameters) Habitat Yes No P ¼ 0.58 Aquatic 30 1 Terrestrial 23 2 Order Yes No P ¼ 0.31 Invertebrates 10 0 Fishes 24 1 Amphibians 2 0 Reptiles 4 1 Birds 8 0 Mammals 5 1 Sense Yes No P ¼ 0.33 Vision 44 2 Auditory 7 1 B. Number of studies testing the second component of Sensory Drive (Signalling traits varying by environmental parameters) Habitat Yes No P ¼ 0.0036 Aquatic 30 0 Terrestrial 74 19 Order Yes No P ¼ 0.0055 Invertebrates 14 6 Fishes 27 0 Amphibians 12 6 Reptiles 10 0 Birds 32 6 Mammals 9 1 Sense Yes No P < 0.0001 Vision 59 1 Auditory 40 18 Figure 2. Frequency wafﬂe plots of studies supporting and not supporting the C. Number of studies testing both components of Sensory Drive (sensory sensory drive model by aquatic (red) or terrestrial (orange) habitats, including and signaling coevolution) studies that evaluated the sensory component of the sensory drive model, Habitat Yes No n.a. studies that evaluated the signaling components of the sensory drive model, Aquatic 18 0 and studies that evaluate the complete model (both major components). Note Terrestrial 11 0 for color blind readers (either deutanomaly or protanomaly) the aquatic Order Yes No n.a. blocks will appear a dark green and the terrestrial a dark yellow). Invertebrates 5 0 Fishes 16 0 Amphibians 1 0 Evidence for the environment influencing signal Reptiles 4 0 components Birds 3 0 Our literature search found more than twice the number of studies Mammals 0 0 Sense Yes No n.a. exploring the signal components of the sensory drive model than Vision 25 0 the sensory components (Table 1, Figures 2–4). We identified 126 Auditory 2 0 empirical studies that directly tested the signal predictions of the sensory drive model (blue components in Figure 1). Of these studies, Note vibratory studies listed in Table 1 are excluded for this analysis; and n.a. 107 found support for sensory drive while 19 did not. Many refers to inapplicability of the statistical test when only 1 column has numbers researchers have tested this part of sensory drive by examining cor- > 0. relational patterns between male signaling characteristics and envir- onmental parameters (Table 1: Morton 1975; Gish and Morton 1981; Reimchen 1989; Wiley 1991; Fleishman 1992; Marchetti 1993; Seehausen et al. 1997; Slabberkoorn and Peet 2003; Fuller and Nelken 2007; Mockford and Marshall 2009) are modified by 2002; Leal and Fleishman 2004; Gomez and The ´ ry 2004, 2007; Ord background noise levels. Auditory systems can be selectively tuned et al. 2007; Stuart-Fox et al. 2007; Gray et al. 2008; Derryberry to respond to conspecific signals (e.g., auditory imprinting, Batista 2009; Ey et al. 2009; Elias et al. 2010; Morrongiello et al. 2010; et al. 2016), as well as be modified by steroid hormones (Coffin Tobias et al. 2010; Potvin et al. 2011; Hancox et al. 2013; Brock et al. 2012). And some of the best examples of sensory tuning to the et al. 2017); or species-specific detection biases (Madden and environment include the evolution of selective ultrasonic hearing Tanner 2003; Feng et al. 2006; Cummings 2007; Arnqvist and Kolm capabilities among several species preyed upon by echolocating bats 2010), or female mate preference functions (Boughman 2001; Maan (Conner 1987; Windmill et al. 2006). et al. 2006; Seehausen et al. 2008; Kelley and Endler 2012). Downloaded from https://academic.oup.com/cz/article-abstract/64/4/471/5034003 by Ed 'DeepDyve' Gillespie user on 22 August 2018 478 Current Zoology, 2018, Vol. 64, No. 4 (Figure 2). This is a reverse pattern from the relative habitat repre- sentation observed for sensory component studies (Figure 2). Why the difference? The difference may be a matter of human acces- sibility between these two habitats. Or simply driven by the taxo- nomic foci of different researchers (e.g., birds, reptiles, amphibians, and several invertebrate orders are not found in the sea). In addition, acoustic signaling is far more common in the terrestrial environment than the aquatic environment, allowing signal researchers a broader range of signal forms to study. While recent research is beginning to discover the broad range of underwater sounds (Smith and van Staaden 2009; Danley et al. 2012), the field of underwater acoustics is still nascent relative to the long history of studying amphibian, bird, and insect calls in terrestrial habitats. 3.4 Auditory signals and the biotic versus abiotic design pressures The terrestrial environment significantly dominated the category of non-supporting sensory drive studies concentrating on signal components (P ¼ 0.0036, Table 2). The high concentration of these non-supporting studies involved auditory signals, a pattern that sig- nificantly deviated from random expectations (P< 0.0001; Table 2). Why do we find a disproportionate number of auditory studies (of which most are in terrestrial environments) representing this cat- egory of no support for sensory drive? One important feature to consider is how sensory modes differ; auditory signals frequently compete simultaneously with both biotic and abiotic noise. Unlike a visual signal, which is directional and whose detection is based on how it is perceived against highly localized abiotic backgrounds (the adjacent surrounding area), auditory signals are essentially omnidir- ectional so it is more difficult to disentangle them from background noise coming from all directions. It is the competition to stand out against the biotic din of competing signals that has been shown to Figure 3. Frequency wafﬂe plots of studies supporting and not supporting the be the dominant predictor of divergence in a number of different sensory drive model by sensory modality [vision (red), auditory (orange)] auditory signalling systems (e.g., insects: Greenfield 2015; frogs: including studies that evaluated the sensory component of the sensory drive Wollerman and Wiley 2002; Ame ´ zquita et al. 2011; Malone et al. model, studies that evaluated the signaling components of the sensory drive 2014; birds: Luther 2009; Grant and Grant 2010). As a general rule, model, and studies that evaluate the complete model (both major compo- acoustic signal reception has to contend with significantly more bi- nents). Note for color blind readers (either deutanomaly or protanomaly) the vision blocks will appear a dark green and the auditory a dark yellow). otic interactions than visual signals. Hence, signal design in ecosys- tems crowded with auditory communicators should be associated with the biotic environmental soundscape being the better predictor Still others have focused on the time and place of male signaling, to for signal differentiation than the abiotic factors. This has been born determine whether or not signaling behavior maximizes conspicu- out in a number of different animal taxa (Ame ´ zquita et al. 2011; ousness to females (Endler and The ´ ry 1996; Long and Rosenqvist Wilkins et al. 2013). One of the most thorough examinations of 1998; Doucet and Montgomerie 2003; Heindl and Winkler 2003; this principle comes from a large-scale comparison of 82 species of Lardner and Lakim 2002; Uy and Endler 2004; Sun and Narins tropical forest birds, wherein Luther (2009) found that bird song 2005; Heinsohn et al. 2005; Ord et al. 2007; Peters et al. 2007; divergence at dawn chorus was predicted by the composition of Rutkowski et al. 2007; Chapman et al. 2009; Cole and Endler competing songs at each given time interval, rather than physical 2016). location or phylogenetic relatedness. Hence, for auditory signaling, Of the supporting studies, 71% were in terrestrial systems the communication environment is often dominated by biotic fac- (Figure 2), 57% involved visual signaling (Figure 3), and taxonomic tors more than abiotic features, and it is the selective factor driving representation was quite broad (31% birds, 26% fish, 13% inverte- signal diversification in predictable directions. However, auditory brates, 12% amphibians, 10% reptiles, and 9% mammals, evolution may be less predictable than visual signal evolution be- Figure 4). All of the 19 studies finding no support for sensory drive cause the auditory biotic factors are often more variable in space, were in terrestrial environments and 95% (18) involved auditory and in both short-term and evolutionary time, than the largely signals across three taxonomic groups (invertebrates, amphibians, physical factors affecting vision. and birds). Comparing the supporting and non-supporting studies (Table 2), we found significant non-independence of support by Evidence for complete sensory drive model habitat (P ¼ 0.0036), modality (P< 0.0001), and taxon (P ¼ 0.0055). (co-evolution of sensory and signaling features) The terrestrial environment dominated the studies finding Of the 154 studies examining sensory drive processes, 29 tested and support for the signal components of the sensory drive model found support for the complete sensory drive model (Table 1). Downloaded from https://academic.oup.com/cz/article-abstract/64/4/471/5034003 by Ed 'DeepDyve' Gillespie user on 22 August 2018 Cummings and Endler. Sensory drive evidence and its watery bias 479 Figure 4. Frequency wafﬂe plots of studies supporting and not supporting the sensory drive model by taxonomic group [supporting (red) and non-supporting (orange)] including studies that evaluated the sensory component of the sensory drive model, studies that evaluated the signalling components of the sensory drive model, and studies that evaluate the complete model (both major components). Note for color blind readers (either deutanomaly or protanomaly) the sup- porting blocks will appear a dark green and the non-supporting a dark yellow). Either tests not supporting the full model haven’t yet been conducted well. The Lake Victorian cichlids differ in optical environment due or the authors could not publish their negative results. The support- to a predictable (and unidirectional) change in ambient spectra with ing studies were overwhelmingly focused in visual traits (86%, depth. As species-specific depth ranges increase, ambient spectral Figure 3) with a bias for aquatic environments (62%, Figure 2) and bandwidth becomes narrower and redder. In this system, visual pig- a majority (55%, Figure 4) of fish representatives [followed by ments follow this depth gradient shift as well as predictable shifts in invertebrates (17%), reptiles (14%), birds (10%), and amphibians male color reflectance to contrast against the shift in background (3%)]. spectra (Seehausen et al. 2008) that is also reflected in female choice The close similarity between characteristics of studies finding for these signals (Maan et al. 2006). Meanwhile, in the Lake support for sensory components and the complete sensory drive Malawi cichlids that inhabit clearer waters with a broader spectrum model is not surprising. After all, the sensory drive model starts with of ambient light, the optical environment is less constrained, and the the environment placing a directional change on sensory systems in multiple (6 main opsins) show no correlated pattern with expression specific environmental conditions. To find evidence for the complete and optical environment (Smith et al. 2012). This point was brought Sensory Drive model, one needs to first find a match between sen- up by Endler in the early stages of Sensory Drive (Endler 1993a, sory system bias predicted by environmental constraints and then a 1993b), that environments that are optically constrained to narrow match between signals and that environmentally induced sensory irradiance spectra favor a very specific color component for signal bias. To tackle both components is a daunting endeavor, so it should evolution, whereas environments containing broad spectra are very come as no surprise that the subset of studies that completed this permissive, favouring diversity and making predictions more diffi- challenge is not very large (about 1 per year since the inception of cult. This same principle explains why there is strong support for Sensory Drive). sensory drive in the surfperch fishes optically extreme environment It is also not surprising that the majority of these few “full sup- of an underwater kelp forest (Cummings 2007), yet more muted port studies” are mostly in aquatic environments. Since the early support in birds dwelling in tropical terrestrial forests (Gomez and days of sensory drive, it was noted that aquatic environments place The ´ ry 2004; Maia et al. 2016). a more constraining force on the sensory environment than terres- trial habitats, particularly in visual systems. The water medium, unlike air, differentially absorbs and scatters wavelengths of light as Conclusions and Future Directions a function of depth as well as biotic and abiotic factors in the water medium itself, such as tannins. Phytoplankton and zooplankton There is broad support for the process of sensory drive in a variety blooms along with detritus and other inorganic materials can also of taxa and environments but the distribution among taxa and envi- stain the waters in particular ways, leaving a very limited optical ronments is uneven. The unevenness results from variation among spectrum for the visual senses to process. When spectra are habitats as well as in sensory capacities and sensory biophysics. restricted, then sensory systems have fewer options for tuning and Some combinations restrict what form sensory drive can take, the predicted direction of tuning and signals becomes predictable making it predictable, but other combinations are very permissive, based on first principles. However, when the spectrum is broad, the making predictions difficult or impossible. There may even be a system is permissive and multiple solutions are equally plausible tradeoff between environmental constraints and diversity. This pre- (Endler 1993a,1993b). dicts more diversity of senses and signals, and more diversity of spe- A comparison across the different types of cichlid fish and the cies, in permissive habitats and species with multiple sensory modes optical environments they inhabit demonstrate this principle quite than those with fewer modes or which live in more restrictive Downloaded from https://academic.oup.com/cz/article-abstract/64/4/471/5034003 by Ed 'DeepDyve' Gillespie user on 22 August 2018 480 Current Zoology, 2018, Vol. 64, No. 4 Brumm H, Voss K, Kollmer I, Todt D, 2003. Acoustic communication in habitats. These ideas need testing in as many taxa and habitats as noise: regulation of call characteristics in a New World monkey. J Exp Biol possible. We also note that there is comparatively little work on sen- 207:443–448. sory drive in chemoreception, vibration reception, and electrorecep- Carleton KL, Kocher TD, 2001. 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Published: Aug 1, 2018
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