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Visual floral traits, flower color in particular, are important features that shape plant interactions with the surrounding environment (Schaefer and Ruxton, 2011; Willmer, 2017). Flowers show enormous variation in color among closely related taxa, and even between or within natural populations of the same species (i.e., flower color polymorphism) (Gigord et al., 2001; Warren and Mackenzie, 2001; Narbona et al., 2018; Souto-Vilarós et al., 2018). The factors that drive flower color evolution in highly diverse genera or families, particularly within a species, remain an open area of research.

Flower color is one of the most important characters for signaling to animal pollinators (Schiestl and Johnson, 2013). Therefore, pollinators are often perceived as one of the primary selective agents influencing flower color. Differences in the visual capabilities of pollinators can impose variable selective pressure on flower color, leading to variation (Wester and Lunau, 2017; de Camargo et al., 2019). In some plant species color transitions represent an adaptation to different, sometimes new, suites of pollinators (Armbruster et al., 2000; Fenster et al., 2004). For instance, in some plant genera, color is the best predictor of a transition between insect and bird pollination (Sutherland and Vickery, 1993; Roguz et al., 2018).

While flower color is a central visual cue to animal pollinators, the floral reward also plays a key role in shaping the interaction (Roy et al., 2017; Parachnowitsch et al., 2018; Roguz et al., 2018, 2019). Typically, plants provide a food reward of either pollen or nectar. Of these, nectar is perhaps the most important in an evolutionary sense (Simpson and Neff, 1983; Canto et al., 2011). Although it is a strong attractant, producing nectar is physiologically costly, and thus in several cases, the ability of flowers to produce nectar has been lost (Little, 1983; Dafni, 1984; Sletvold et al., 2016). In some plant families, e.g., Orchidaceae, the presence or absence of a nectar reward may be correlated with flower color. Non-rewarding, sexually deceptive orchids often have brightly colored flowers (Spaethe et al., 2010), while species with nectar often have green or white colored flowers (Duffy and Stout, 2011). The lack of a food reward might result in, or be the result of, the development of new rewarding characters that attract potential pollinators. These new attractants may include changes in flower color and size (Gigord et al., 2001; Vereecken and Schiestl, 2009). For example, night-sheltering reward systems without a food reward are often associated with large, dark flowers (Dafni et al., 1981; Sapir et al., 2005, 2006; Watts et al., 2013; Lavi and Sapir, 2015). Dark petals with their highly absorptive surfaces may result in higher temperatures inside the flower, which may benefit flower visitors (Sapir et al., 2006; Watts et al., 2013). As a result, in such systems flower size and color, but not food rewards, are typically under strong selection (Vereecken et al., 2013; Lavi and Sapir, 2015; Pellegrino et al., 2017).

Flower color changes might also be associated with a shift in plant mating system (Landis et al., 2018). The majority of flowering plants have both male and female reproductive parts, however, the mutualistic interactions with pollinators enable most of these plants to outcross (Goldberg et al., 2010). Shifts in flower color and pollination vectors may result in changes in mating system (i.e., selfing or outcrossing). Some species that rely on pollinators have lost the ability to self-fertilize, becoming self-incompatible, while in other cases the reverse occurred (Landis et al., 2018). Strong selection on floral traits, including color, is expected in self-incompatible taxa relying completely on animal-mediated pollination. Whereas in self-compatible taxa, this animal-mediated selection is expected to weaken since pollinator visitation may no longer be required for reproduction (Anderson and Busch, 2006). Thus, while pollinators often play a critical role in the evolution of flower color, this may not always be the case.

Plants experience a myriad of interactions with animals, both mutualistic and antagonistic. The strength and direction of selection that these agents exert on flower color may differ (Irwin et al., 2003). For example, flower color may have evolved as an adaptation against fungi and/or herbivores (Chalker-Scott, 1999; Chittka and Schürkens, 2001). Irwin et al. (2003) found that herbivores and pollinators exert opposing selection on flower color in Raphanus sativus. In this system, because both herbivores and pollinators prefer lighter flowers, dark flowers persist, thus maintaining a stable color polymorphism.

In some taxa, however, there is little or no association between color and interacting animals (Armbruster, 1996). Instead, variation in pigmentation within and among closely related taxa may be maintained by selection related to environmental heterogeneity (Warren and Mackenzie, 2001). The three main groups of pigments responsible for color in plants, flavonoids, carotenoids and betalains, play a functional role in plant physiology (Schaefer and Ruxton, 2011). Flavonoids, for example, are known to function as a response to plant stress caused by drought (Warren and Mackenzie, 2001), cold (Chalker-Scott, 1999; Harborne and Williams, 2000), and nitrogen deficiency (Bonguebartelsman and Phillips, 1995). They also protect plants against damage caused by UV radiation or visible light (Chalker-Scott, 1999; Tanaka et al., 2008). Flower color mediates plant interactions with both the abiotic and biotic environment, and thus exploring the drivers that lead to flower color diversity is of key importance to understand the evolution of plant diversity.

Transitions in flower color are common across the phylogenies of Angiosperm lineages (Streisfeld and Rausher, 2011; Wessinger and Rausher, 2012, 2014; Martins et al., 2016; Roguz et al., 2018). The diversity of flower color among and within these modern lineages suggests that most of these transitions must have been adaptive (Rausher, 2008). While the mutations causing flower color shifts are well understood at the biochemical level (Grotewold, 2006), the broader macro-evolutionary drivers of flower color diversity have only been studied in few plant groups (Landis et al., 2018; Ng and Smith, 2018). To understand these macro-evolutionary forces, we need to explore plant lineages exhibiting a diversity of flower colors.

The genus Iris is one of the most diversified genera in Asparagales. Iris comprises over 300 species (Royal Botanic and Gardens, 2020), which are widespread throughout the Northern Hemisphere (Goldblatt and Manning, 2008), with the greatest number of endemics occurring in the Mediterranean and Asia (Wilson, 2006). Although some irises are found in mesic or even wetland environments, most species grow in desert, semi-desert, or dry, rocky, montane habitats (Wilson, 2006). Members of this genus display a remarkable variety of flower colors, ranging from extremely dark, purple flowers, through violet and pink, to yellow and white flowers (Mathew, 1989; Sapir and Shmida, 2002; Sapir et al., 2002). This dazzling palette of colors and patterns seen in Iris flowers may be associated with their wide variety of life histories, pollination and mating systems, and habitats. Thus irises represent an outstanding model to study evolutionary biology and speciation in plants, especially in the context of flower color (Crespo et al., 2015).

To understand the unusual flower colors and color patterns in irises we investigated the evolution of flower color and several related traits, including pollinator type, nectar reward, and mating system, across the entire phylogeny and geographic range of the genus. By determining the ancestral state of Iris traits and comparing it to the traits of modern species, we should be able to shed light on which traits are the causes and which are the effects. To this end, we asked the following specific questions, first, what was the ancestral state of flower color and related traits in Iris, and second, are floral trait transitions from ancestral to modern states better explained by environmental or pollinator mediated selection?

Iris flowers display a wide diversity of colors and color patterns among and within species. The diversity seen in modern irises is the result of several changes over evolutionary history in the genus. In this study, we reconstructed the traits of the most recent common ancestor of the Iris genus. This ancestor likely had monomorphic, one-colored purple flowers, with a crest and a spot on the falls. The flowers were likely insect-pollinated, nectar-rewarding, and self-compatible. Since then, the genus has diverged to include over 300 taxa that exhibit a wide range of colors and patterns, including polymorphic, continuous, and bi-colored flowers. Additionally, some taxa now have a beard, instead of a crest, have lost the spot (and sometimes regained it), and some are now self-incompatible and rewardless. There have been a few shifts from insect-pollination to bird-pollination, and occasionally back again. Thus, by comparing these derived states to the ancestral state, and placing them in the context of the Iris distribution and reproductive system, we can infer some of the drivers of floral color diversity in Iris.

Flower color is the most variable trait of those we studied in the genus Iris. Some of that diversity is likely the result of mutations, which can cause up- or down-regulation of specific genes, leading to differences in the amount of synthesized pigment and in color shades (Durbin et al., 2003). The correlation between flower color diversity and anthocyanin synthesis is common not just in Iris, but across many genera, e.g., Petunia and Ipomea (Durbin et al., 2003). Unlike some of the other groups, however, the flower color diversity in Iris is not just related to the presence or absence of anthocyanin pigments, but also the result of variation in colors produced by anthocyanins (Warren and Mackenzie, 2001). Moreover, in Iris we also observed many cases of bi-colored flowers, which may be the result of tissue-specific variation in anthocyanin production, or the loss of anthocyanins in the standard or the fall.

Color polymorphism, continuous coloration, and bi-colored flowers arose multiple times across the Iris phylogeny, and many are maintained to this day (Wang et al., 2016). The maintenance of color polymorphism is not common in other genera. Typically, one of the color morphs will eventually be lost and the taxa will again be monomorphic (Ellis and Field, 2016). The maintenance of stable color polymorphism, and other color variations, in Iris may be caused by an absence of selective disadvantage on color in these taxa or by stabilizing selection exerted by multiple agents (reviewed in Sapir et al., in review). For example most populations of I. lutescens and I. pumila are polymorphic and neutrally distributed in space (Wang et al., 2016), but in some populations color variation may be due to divergence (Souto-Vilarós et al., 2018). Several factors may maintain this neutral distribution, including environmental heterogeneity (Tucić et al., 1998). Additionally, while selection should lead to the fixation of one color morph, polymorphism may also be maintained over the long-term due to perennial life history and vegetative reproduction, which cause generation overlap in many Iris species (Gray and McKinnon, 2007).

Almost half of the studied Iris taxa produce white morphs, which is a common color-transition in many angiosperm taxa, resulting from shut-down of genes in the pigment biosynthesis pathway (Wessinger and Rausher, 2012). However, the modern Iris taxa with (only) white-colored flowers can be found in the subgenera Scorpiris and Limniris. For some Iris species white flowers may be an evolutionary dead-end, without possibility for reversal. Pigment loss may alter pollinator attractiveness (Waser and Price, 1981) or reduce the capacity to deal with environmental stress, such as drought (Ellis and Field, 2016), or a combination of the two (Warren and Mackenzie, 2001).

Like the high diversity of flower color and patterns seen across Iris taxa, corolla diameter seems to be fairly variable across the phylogeny. The visual attractiveness of flowers is substantially related to flower color and size. Although large flowers are costly (Teixido et al., 2016; Roddy, 2019), some of the species with large flowers in the genus Iris grow in desert or semi-arid habitats. This suggests that pollinator-mediated selection is more important in driving the evolution of large flowers (Lavi and Sapir, 2015; Souto-Vilarós et al., 2018). The strategy to produce big, showy, self-compatible flowers with lots of nectar is found in most Iris taxa and may increase mating success, especially when florivory is not a threat (Ghara et al., 2017). While positive pollinator-mediated directional selection on flower size may be a factor in some Iris taxa (Lavi and Sapir, 2015; Souto-Vilarós et al., 2018), this is not always the case (Ishii, 2005; Pellegrino, 2015).

Most Iris species are pollinated by insects, but in a few cases, shifts to bird pollination evolved. Several taxa of Iris have blue-violet or purple flowers, which tend to be associated with bee visitation because bees tend to have an innate preference for the blue range of wavelengths (Lunau and Maier, 1995; Dyer et al., 2015). Bees also have an innate preference for yellow flowers, and thus the common shift from purple to yellow flowers in Iris may be maintained by bee preferences (Giurfa et al., 1995; Lunau and Maier, 1995; Spaethe et al., 2001). This innate preference for both purple and yellow flowers may explain the equal seed set between color morphs in some polymorphic Iris populations (Imbert et al., 2014a, b; Souto-Vilarós et al., 2018).

Bird-pollinated flowers tend to be red or orange (Rodríguez-Gironés and Santamaría, 2004; Cronk and Ojeda, 2008), and these two colors have arisen several times in the Iris phylogeny. Red coloration may be a good predictor of bird-pollination in irises, but not vice-versa. There is only one taxon with red flowers, and it is bird-pollinated (I. fulva, Emms and Arnold, 2000; Martin et al., 2008), but other bird-pollinated species are not red (e.g., I. missouriensis, Lyon, 1973). This suggests that color is likely not the major trait driving pollinator-shifts from insects to birds in Iris. All the bird-pollinated taxa have wide, open and flat flowers that produce dilute nectar (Wesselingh and Arnold, 2000). Being able to access the flower (wide open, flat flowers) and obtain the preferred food reward (diluted nectar) seems likely to be the trigger for the transition to bird pollination. Shifting from purple to red flowers may be relatively easy because the anthocyanin biosynthesis pathway is relatively flexible (Warren and Mackenzie, 2001; Albert et al., 2011). Bird-driven transitions from purple to red flowers, however, would likely be countered by insect pollination because insects often prefer blue-violet (Lunau and Maier, 1995; Dyer et al., 2015) and yellow flowers (Giurfa et al., 1995; Lunau and Maier, 1995; Spaethe et al., 2001). This may explain why two out of the three extant bird-pollinated flowers are purple, and not red.

We found a strong signal for the association among floral structure, reward, and mating system. All taxa have either a crest or a beard, but never both. Although the ancestral Iris probably had a crest, the beard replaced the crest relatively early in the common ancestor of Oncocyclus, Pogon, and Regalia. Around the same time, this group of subgenera also lost the ability to produce nectar and became self-incompatible. Once the transition to a beard and self-incompatibility occurred in this section, it never changed back. In contrast, nectar production was regained several times. We also found, that white-purple and purple flower color, which are commonly found among members of these subgenera, are associated with self-incapability and a lack of nectar. While the association of these traits and their strong phylogenetic signal suggests the evolution of a monophyletic pollination syndrome, it is important to note the sampling of these traits was not similar across all species.

Nectar production requires regular and consistent water availability. In the dry regions inhabited by Oncocyclus, Pogon, and Regalia irises, water limitation could have been the agent of selection against nectar production, leading to the loss of this trait in their common ancestor. Once these irises became nectarless, the question becomes: how did they attract insect pollinators? Potentially, this is when the night-sheltering reward system, that is well-described in the Oncocyclus group, arose (Sapir et al., 2005; Monty et al., 2006; Vereecken et al., 2013; Watts et al., 2013). Oncocyclus irises are primarily pollinated by male Eucera bees (Apidae, Eucerini) that shelter in the flowers overnight (Sapir et al., 2005, 2006; Watts et al., 2013). Pollination occurs as the male bees visit multiple flowers before choosing the flower in which they will spend the night (Sapir et al., 2005; Monty et al., 2006). While it is possible that bees slept in the flowers before nectar was lost, after nectar-loss the sheltering component became the only reward. Thus, shelter may have become a replacement mechanism to attract pollinators.

The loss of nectar is associated with the transition from crest to beard. If a crest serves as a nectar guide, there will be no selection to maintain it in nectarless species. Instead, a beard might have selected by its advantage in alternative reward types, such as the derived sheltering-reward system. The role of the beard remains debatable, but it would be interesting to test whether the presence of a beard changes the airflow over the fall and impacts the rate of warming in these flowers, or whether it contributes for pollen deposition on stigma.

Another open question is why self-compatibility only arose in the closely related Oncocyclus, Pogon, and Regalia (except for I. tenuis). The loss of self-compatibility seems risky, but perhaps it was necessary to maintain genetic diversity. Most of the taxa in these subgenera occur in highly variable habitats in the Middle East and Western Asia. In a complex habitat mosaic, with patchy and extreme environmental conditions, being self-compatible may be maladaptive. Self-compatibility would naturally lead to selfing and inbreeding, thus reduce genetic diversity. Maintaining genetic diversity is particularly important for plants in highly variable and stressful conditions. It facilitates quick adaptation and increased population persistence, as a sort of insurance. Indeed, most of these taxa have highly variable flower traits, most notably in terms of color.

The nectarless Oncocyclus, Pogon, and Regalia, tend to have high levels of color polymorphism, continuous color variation, and bi-colored flowers. Within-species variation in flower color may be important in deceptive systems, since it impedes the learning ability of pollinators and leads to negative frequency-dependent selection (Smithson and MacNair, 1997; Gigord et al., 2001; Imbert et al., 2014a). Another strategy to maintain the attractiveness of no-food rewarding species is flowering early in the season and attracting naïve pollinators (Imbert et al., 2014a). In any case, it is surprising that more taxa in these subgenera did not regain nectar production. Comparative studies have shown that nectarless taxa in general (Aragon and Ackerman, 2004; Sletvold et al., 2016), and Iris taxa specifically (Lavi and Sapir, 2015; Souto-Vilarós et al., 2018), are much more pollen limited than nectar producing taxa.

Irises cover a broad geographic range across a mosaic of habitat types, environmental stresses and pollinator types, which is likely the ultimate cause of the observed flower diversity. In general, some Iris taxa seem to have strong pollinator-mediated selection on floral traits, such as color and size. In other taxa, however, the environment seems to play a stronger selective role in one or more of these traits. The diversity of flower colors we see in Iris, likely represents a trade-off between conflicting selection pressures (Souto-Vilarós et al., 2018). Whether changes in flower color are the result of neutral processes without any selection, or whether these changes are tightly maintained by abiotic or biotic selective agents, remains an open question.

All datasets generated for this study are included in the article/Supplementary Material.

YS and KR conceived and designed the research. KR and MG performed analyses. KR, MG, and YS wrote the manuscript, with contributions from all authors. All authors collected the data.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.