The genus Drosophila provides an incredible array of phenotypic, evolutionary and ecological diversity (Jezovit et al., 2017; Keesey et al., 2019; Keesey IW et al., 2019; Markow, 2015; Markow and O'Grady, 2007; O'Grady and DeSalle, 2018). Members of this genus, which provides roughly 1500 species including the model organism D. melanogaster, inhabit all continents except Antarctica, and occur in almost every type of environment. Due to their vast variation in behavioral, morphological and natural history traits, the comparison of vinegar flies provides an enormous potential for the understanding of driving forces in evolutionary processes. In particular, the feeding, courtship and breeding sites of this genus are tremendously diverse, including both generalists and specialists, and spanning extreme dietary variation and host utilization such as different stages of fruit decay, as well as flowers, mushrooms, sap or slime flux, rotting leaves, cacti and many other sources of microbial fermentation. It is important to note that preferences in feeding and oviposition have shifted numerous times, and closely related species are known to utilize different types of food resources (Crowley-Gall et al., 2019; Crowley-Gall et al., 2016), or to visit a host at different stages of decay (Karageorgi et al., 2017; Keesey et al., 2015; Ometto et al., 2013). At the same time, it is common to find phylogenetically distant species using the same host, or living in overlapping environments (Hey and Houle, 1987; Lachance et al., 1995; Martin, 1998; Taylor, 1987; Taylor and Powell, 1978). Therefore, the spatial distribution of species over discrete patches of an ecosystem, such as within a temperate forest, might vary according to discrete microhabitats. While little ecological information is available for a majority of the non-melanogaster species, it has been shown repeatedly that many of the members of the obscura species group overlap geographically as well as ecologically in their utilization of temperate forest ecosystems (Bächli et al., 2006; Burla et al., 1986; Michell and Epling, 1951). Moreover, these local environments may create different selective and energetic pressures for neuroanatomy (Niven and Laughlin, 2008) that in turn could provide an opportunity and rationale for the coexistence of many species within a single habitat or ecological niche (Finke and Snyder, 2008; Griffin and Silliman, 2011).

In an earlier paper, we showed that robust idiosyncrasies exist between visual and olfactory investment across this genus (Keesey et al., 2019), including many examples of inverse variation within a subgroup, and between sympatric species and subspecies that utilize seemingly identical host plants or food resources. However, most vinegar fly species have an understudied ecology, and other than information about where and when they were collected for laboratory establishment, we often know very little about their natural habitats or ecological preferences. The aim of the present paper is to determine whether behavioral, phenotypic, and neuronal differences between close relatives all combine to support the coexistence of different species within a single ecological habitat. As predicted by our initial hypotheses, we document that these sensory traits vary significantly between two close relatives within the obscura group – D. subobscura and D. pseudoobscura – and we examine in detail the potential driving forces of speciation, such as biotic and abiotic factors, including courtship modalities and phototactic response. Next, we expand our research objectives to predict sensory variation in monophyletic species based on our hypothesis from the obscura group, including D. persimilis, D. affinis and D. bifasciata, where we test our hypothesis that this sensory variation will consistently occur across subgroups within the obscura clade. Here, we assert that even between close, phylogenetic relatives as well as sympatric species, these differences in visual and olfactory sensory investment are strongly apparent. We propose that these sensory differences could reduce interspecies competition via resource partitioning and through innate variation in microhabitat or microclimate preferences, thus promoting speciation, novel niche establishment, as well as stabilizing selection using natural sensory trait variation across this important genus of insects. Moreover, behavioral differences related to phototaxis appear to be more significant between sympatric species, and thus niche partitioning may be the initial driving force, whereas differences in courtship then promote and maintain speciation events.

When we imagine examples of isolation barriers, we often consider those that are distinctly physical in nature, such as a mountain range or a remote island biogeography. However, sensory isolation barriers also exist, including differences in pheromone chemistry between geographically overlapping species (Chung et al., 2014; Löfstedt, 1993; Löfstedt et al., 1991; Mitchell et al., 2015), or variations in the songs and auditory repertoires of crickets, frogs and birds (Blair, 1974; Hobel and Gerhardt, 2003; Kirschel et al., 2009; Walker, 1974). In this study, we hypothesize that sources of light gradients may also create strong selective pressures and isolation mechanisms that in turn lead to speciation events or stabilizing selection for opposing phototaxis within otherwise overlapping habitats, such as arboreal forests. Moreover, we propose that these light gradients most likely work in tandem with inverse changes in pheromone or chemosensory changes to further provide avenues for species divergence. Arboreal forest microhabitats have been addressed previously as sources for spatial separation between species (Atkinson and Miller, 1980; Montgomery and Merrill, 2017; Penariol and Madi-Ravazzi, 2013; Taylor and Powell, 1978), including studies directly related to the field-sampling of members of the family Drosophilidae, often with the division of species occurring in proximity to the forest edge. While the evolutionary selective pressures and their effects on the relative size of various components of the nervous system have not been previously examined, it has been suggested that sources of light may be one of the ambient forces driving the observed tradeoff in the evolution of these two sensory structures (Keesey et al., 2019). However, additional field studies are still needed to confirm whether these sensory investments differ outside the laboratory, and to examine how insect species sort in the wild, for example, via niche partitioning or character displacement.

Here we demonstrate that several monophyletic species within the obscura group, despite being close relatives, deviate significantly in regards to both eye and antenna morphology (Figure 1), as well as in their corresponding neuropils for vision and olfaction (Figure 2). In addition, we observe that this variation in sensory systems positively correlates with both courtship behavior (Figure 3) and environmental habitat preferences (Figure 4), especially as related to the relative importance of visual stimuli or sources of light, which appears to be of opposing value between these sibling species (Figure 5). Previous work has documented this tradeoff or inverse resource allocation between vision and olfaction across more than 60 species within the Drosophila genus (Keesey IW et al., 2019), but the ecological mechanisms and selective pressures underlying this divergence have not been studied as explicitly in monophyletic species groups or subgroups. While little ecological information is available for a majority of the non-melanogaster species, it has been shown repeatedly that many of the members of the obscura species group overlap geographically as well as ecologically in their utilization of temperate forest ecosystems (Bächli et al., 2006; Burla et al., 1986; Michell and Epling, 1951). In addition, there has been documentation of a recent geographical overlap between D.pseudoobscura and D. subobscura in North America, which might make for an ideal field study in the future to test our hypotheses regarding environmental partitioning and the evolution of sensory variation (Noor, 1998; Pascual et al., 1998). However, the species D. pseudoobscura and D persimilis have been well established as sympatric (Crysnanto and Obbard, 2019; O'Grady, 1999), and already act as models for genetic variation in phototaxis and courtship (Brown, 1965; Brown, 1964; Hernández and Fabre, 2016; Noor and Aquadro, 1998; Ripfel and Becker, 1982). However, these behaviors have not been previously studied concurrently, nor with the overlay of morphological and neurobiological data across both visual and olfactory sensory systems. In these two evolutionarily sympatric species (i.e. D. pseudoobscura and D persimilis), we demonstrate significant deviation in visual and olfactory behavior, including both phototactic response and potential visual bias during male courtship (Figure 5D–G), thus supporting our initial proposal that variance in sensory investment occurs even within closest, sympatric species across this genus. While we have sampled several species, it would also be important to address additional Drosophila species within the obscura group, such as D. tristis, D. tsukabaensis, D. obscura, D. miranda, D. iowei, D. ambigua and D. helvetica. This is especially true in cases where these species potentially share ecological overlap in habitat utilization or geography, and where genomic information is perhaps readily available for additional analyses of the molecular mechanisms for this sensory tradeoff (Ramaekers et al., 2019). In the present study, we test the hypothesis that close insect relatives may divide host or habitat resources through niche partitioning by inversely prioritizing the relative importance of visual stimuli as compared to those stimuli that are olfactory. This explanation would be consistent with previous observations that monophyletic species often possess inversely correlated eye and antenna sizes despite being close relatives and despite sharing seemingly identical hosts and environmental preferences (Gaspar et al., 2020; Keesey et al., 2019; Özer and Carle, 2020; Ramaekers et al., 2019). In addition, this hypothesis continues to be consistent with the more in depth analyses afforded by the present study, which documents this sensory inversion across the obscura group, including across close, sympatric relatives, as well as across several populations or strains of each species (Figure 5A,B). Please note that surface areas of the various head and thorax, as well as overall body size, were examined for only one strain per species. It thus remains to be confirmed that the observed differences are truly interspecific. Future research should continue to address both interspecies and intraspecies variation in sensory investment, especially as related to both causal agents and genetic underpinnings of this divergence.

Microhabitats often arise in nature, as landscapes are inherently non-uniform (Martin, 1998; Scheffers et al., 2014). These ecological subdivisions have been examined in regards to cline variation or altitude (Griffiths et al., 2005; Michell and Epling, 1951; Parsons, 1991), as well as temperature gradients or differences in water availability (Enjin et al., 2016; Parsons, 1991; Scheffers et al., 2014; Toda, 1992). In addition, several studies have addressed microhabitat variation and its effects on species richness or biodiversity. Moreover, that plant hosts and other nutritional resources such as fungi and yeasts can differ greatly between forest edge and forest interior (Bächli et al., 2006; Łuczaj and Sadowska, 1997; Penariol and Madi-Ravazzi, 2013; Toda, 1992). Thus, it is well recognized that flora and fauna can vary in both their relative abundance as well as their innate preferences across microclimates within a single habitat, where the fitness of a Drosophila species is intimately tied to its ability to compete for resources within its own environmental niche (Koerte et al., 2020; Qiao et al., 2019). However, the mechanisms by which these innate animal preferences for microhabitats can generate evolutionary pressures or speciation events has not been as thoroughly documented, least of all in a set of model organisms where robust molecular genetic toolkits are available, such as those afforded by the Drosophila genus.

Other insects have been examined for their differences in circadian rhythm or phenology, either in regards to host search or mating behaviors, where close relatives are able to reduce competition by varying their activity cycles (Mitchell et al., 2015). Conversely, it has been well-documented that both D. pseudoobscura and D. subobscura share similar crepuscular activity (Atkinson and Miller, 1980; Bächli et al., 2006; Michell and Epling, 1951; Noor, 1998). Thus, at this juncture we do not feel that the circadian rhythms or seasonal activities of feeding or courtship play any distinct role in the observed evolutionary divergence in relative eye or antenna size. As such, while the light-dependent courtship of D. subobscura suggests a difference from that of D. pseudoobscura in daily patterns of mating, this has not been shown (Atkinson and Miller, 1980; Michell and Epling, 1951; Noor, 1998). Thus, we suggest that it is more likely that D. subobscura simply uses consistent visual stimuli as a species-defining trait, perhaps initiated via a preference for a better-lit arena to perform their courtship ritual and to attract a potential mate. This would include such microhabitats as a forest edge or an open forest canopy (Figure 4C), where visual elements of courtship such as wing displays would be more optimally employed for species identification and female sexual selection given the increases in light availability. Here, we suggest while these species are assumed to be linked via a forest ecology (Bächli et al., 2006; Burla et al., 1986; Michell and Epling, 1951), that D. pseudoobscura may be more likely to prefer darker, inner-forest habitats, while D. subobscura would prefer the forest edge or sections of open canopies within the same forest environment (Figure 4C). This light preference would therefore create opposing spatial regions of highest abundance, where each species would reduce overlap with the other by tuning their sensory systems towards either larger-eyes and positive phototaxis, or smaller eyes and negative phototaxis. We thus propose that this shift in the nervous system would then affect both courtship and host preference. Here, field studies in the 1980s using baited traps did not find a distinct difference in capture across light versus dark areas for D. subobscura (Atkinson and Miller, 1980). However, as mentioned before, additional fieldwork is still needed to continue to test our hypotheses outside of the laboratory, and within naturally occurring populations, for example, in relation to abiotic measures of light gradients and GPS studies of forest canopy cover, and in locations where several species co-occur. It is important to note that, to our knowledge, of the 1200–1500 species of Drosophila that have been documented, none have been described to be nocturnal (which could be an alternative factor for the evolution of especially large and light-sensitive eyes). Thus, it is reasonable that increases in eye size for this genus correlate so strongly with positive phototaxis and correlate with visually mediated courtship (Figure 5F,G), and we propose this occurrence may extend toward all members of the Drosophila genus (Keesey et al., 2019). Moreover, the importance of potential visual displays in courtship and predator avoidance has also been previously examined in some Lepidopterans, including phylogenetic studies across spatial and ecological gradients (Montgomery and Merrill, 2017), as well as in regards to the genetics of wing pigmentation, especially wing spots (Zhang and Reed, 2016). As such, there may be additional factors to address in this interplay between visual and olfactory investment, especially if these same or related genes can be shown to have additional effects beyond the head, for example on the wing pigmentation or across other morphological fodder for evolutionary pressures to exert meaningful sensory changes.

The utilization of forest openings are well studied in avian biology, where males often construct and clear elaborate arenas to perform intricate visual displays for females (i.e. the genus Parotia or six-plumed birds of paradise) (Ligon et al., 2018). However, to our knowledge, the visual capabilities across vertebrate animal species has never been compared to examine evolutionary investments in the nervous system that correlate with visual courtship, and never in regards to alternative sensory methods of courtship such as olfactory or pheromone driven mating rituals. Again, we feel it is likely that investment in the visual system might mirror the tendency of any Drosophila species to possess a positive phototaxis, as all documented species are diurnal. Here we demonstrate that tendency among these five obscura species, although it remains unclear which of these behavioral phenotypes occurs first (e.g. phototaxis or visual courtship), and which behavior subsequently drives a correlation in the other trait over the course of evolutionary time. Using our sympatric species (e.g. D. pseudoobscura and D. persimilis; Figure 5D,F,G), we observe that small changes in morphological investment (EF ratio) correlate with dynamic differences in behavior. Here we note that changes in phototaxis between sympatric species appear to be stronger and more acute than changes in courtship dynamics (Figure 5D,F,G). For example, we observe that the slope of the correlation between phototaxis and EF Ratio for the sympatric species is greater than the slope related to the rest of the obscura subgroup (Figure 5F; orange vs grey). Thus, we hypothesize minor shifts in morphology and neurobiology between sensory components of the nervous system first create exaggerated changes in phototaxis behavior, perhaps due to a spontaneous developmental mutation. This might initially separate species spatially and then subsequently, courtship characteristics start to drift apart (e.g. chemical, auditory or visual cues), which ultimately leads to a division that no longer allows successful mating or progeny to occur and thus that incipient species diverge more permanently.

An alternative hypothesis would be that the phototaxis behaviors may have switched before morphology for some species, through an as of yet unknown mechanism, in order to push these species towards more shaded environments (i.e. perhaps to avoid desiccation pressures). As the visual system is inherently expensive to maintain (Niven and Laughlin, 2008), this could produce a reduction in the visual system, with the evolutionary pressure being energy preservation. Thus, reduction in visual investment would be a consequence, not a driving force, of niche partitioning. This is similar to what occurred within cavefish, where these species living in complete darkness have lost their eyes entirely. However, it is not thought that the fish went to the caves and then speciated as a consequence of losing their vision, rather that the cavefish specialized only after entering into the cave environment, where the no-longer useful eyes were eventually lost. This concept of the evolutionary order of events goes in a direction that remains puzzling across the animal kingdom. Nocturnal animals usually have two pathways for visual investment, either to increase or decrease the eyes. Here, the selection of the preferred visual investment is also not consistent across nocturnal examples, such as owls (large eyes) compared to bats (small eyes). Thus, the evolutionary decision about visual investment seems to rely on the respective starting point for the species or organism, for example if there already has been large visual or auditory investment, then this is perhaps more prioritized over generations. There may also be additional developmental constraints. Moreover, while these cavefish have entirely lost their eyes, as they are in absolute darkness and therefore represent a very extreme habitat example, many deep-sea fish, in direct contrast, have actually increased their eye size investment (e.g. despite the complete darkness), as they perhaps have to observe all manner of bioluminescence. Thus, overall, this is a difficult evolutionary concept to clarify fully, and in absolute terms, especially without more data from additional animal species. Again, we also point out that zero Drosophila species are described as nocturnal, thus variation in eye size may be under significantly different pressures than nocturnal insects, such as crickets (i.e. Orthopterans), which have often greatly increased their visual investment for their nocturnal activity. Here in the present study, we observe that the more significant changes in phototaxis still occur between close, genetic relatives, which appear prior to significant changes in courtship (Figure 5D,F,G). As such, we continue to predict that niche partitioning, character displacement, and response to light gradients are the stronger initial driving forces of the evolution and speciation within the obscura group, where the novel environmental conditions drive sensory investment that in turn optimizes the courtship success of each species in this new niche.

It continues to be unclear which are the most important factors in the visual displays of D. subobscura during courtship, for example, whether outstretched wings provide a specific color or UV pattern (Shevtsova et al., 2011), or whether this wing display simply generates a flash of bright light reflected toward the female (Figure 3B,D,E). Moreover, it has been shown that male D. subobscura do not sing, and thus do not vibrate their wings during display, but we do observe midleg tapping or drumming, which may instead be the auditory component of their courtship ethology. Further work is still needed to qualify and quantify the courtship variation between these species, especially as it pertains to multimodal sensory integration. Thus far, no research has simultaneously compared visual and auditory neurobiology or development for these species, but future work should attempt to encompass these and other sensory modalities. Additional studies will also need to address which photoreceptors are expanded in the compound eye of D. subobscura and how they validate the increases in ommatidium numbers when compared to other close relatives. However, previous research has already shown an expansion of the fruitless positive labeled cells in the optic lobes of D. subobscura as compared to D. melanogaster (Tanaka et al., 2017). Thus, while this pathway has not been addressed yet in D. pseudoobscura or any other members of the obscura group, it is perhaps again indicative of an evolutionary investment in visual modalities for courtship success, given the visual connection to this fruitless labeled neural pathway. Moreover, additional studies should address any sensory investment differences between the sexes, especially given that the fruitless neural network is sexually dimorphic (Gaspar et al., 2020; Tanaka et al., 2017).

Nevertheless, it is apparent from our current data that variation in visual and olfactory sensory system development occurs for more than just mating purposes, and appears to match ecological deviations in behavioral phototaxis and microhabitat preferences for light within a shared ecological niche. In the future, it will continue to be important to test our theories related to niche partitioning as an evolutionary force for speciation across other groups beyond obscura and to continue to provide ecological explanations for the observed variation or tradeoff between these two sensory systems in relation to other geographical overlap and between competing species across the entire genus. In general, additional work is still needed to qualify and quantify the diverse sensory-driven behaviors across this genus of insects, especially as related to their natural ecology and not just laboratory assays, in order to pave the way for future analyses using genetic resources to identify the neural mechanisms governing these morphological and behavioral variations between sensory systems.

All data supporting the findings of this study, including methodology, display examples, raw confocal images and z-stack scans, statistical assessments, courtship videos, as well as other supplementary materials are all available with the online version of this publication. An additional, online data depository also contains raw data from this publication, and this material can be accessed via EDMOND, the Open Access Data Repository of the Max Planck Society (MPG):https://doi.org/10.17617/3.3v.

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Author details

1. Ian W Keesey

   Max Planck Institute for Chemical Ecology (MPICE), Department of Evolutionary Neuroethology, Jena, Germany

   Contribution

   Conceptualization, Resources, Data curation, Formal analysis, Investigation, Visualization, Methodology, Writing - original draft, Project administration, Writing - review and editing

   For correspondence

   ikeesey@ice.mpg.de

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-3339-7249

2. Veit Grabe

   Max Planck Institute for Chemical Ecology (MPICE), Department of Evolutionary Neuroethology, Jena, Germany

   Contribution

   Conceptualization, Data curation, Software, Formal analysis, Investigation, Visualization, Methodology

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-0736-2771

3. Markus Knaden

   Max Planck Institute for Chemical Ecology (MPICE), Department of Evolutionary Neuroethology, Jena, Germany

   Contribution

   Supervision, Validation, Project administration, Writing - review and editing

   Contributed equally with

   Bill S Hansson

   For correspondence

   mknaden@ice.mpg.de

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-6710-1071

4. Bill S Hansson

   Max Planck Institute for Chemical Ecology (MPICE), Department of Evolutionary Neuroethology, Jena, Germany

   Contribution

   Supervision, Funding acquisition, Validation, Project administration, Writing - review and editing

   Contributed equally with

   Markus Knaden

   For correspondence

   hansson@ice.mpg.de

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-4811-1223

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