Increased Floral Divergence in Sympatric Monkeyflowers

Sympatric sister species are predicted to have greater divergence in reproductive traits than allopatric sister species, especially if mating system shifts, such as the evolution of self-fertilization, are more likely to originate within the geographic range of the outcrossing ancestor. We present evidence that supports this expectation-sympatric sister species in the monkeyflower genus, Mimulus, exhibit greater divergence in flower size than allopatric sister species. Additionally, we find that sympatric sister species are more likely to have one species with anthers that overtop their stigmas than allopatric sister species, suggesting that the evolution of automatic self-pollination may contribute to this pattern. Potential mechanisms underlying this pattern include reinforcement and a stepping stone model of parapatric speciation

The case for the continued use of the genus name Mimulus for all monkeyflowers

The genus Mimulus is a well-studied group of plant species, which has for decades allowed researchers to address a wide array of fundamental questions in biology (Wu & al. 2008; Twyford & al. 2015). Linnaeus named the type species of Mimulus (ringens L.), while Darwin (1876) used Mimulus (luteus L.) to answer key research questions. The incredible phenotypic diversity of this group has made it the focus of ecological and evolutionary study since the mid-20th century, initiated by the influential work of Clausen, Keck, and Hiesey as well as their students and collaborators (Clausen & Hiesey 1958; Hiesey & al. 1971, Vickery 1952, 1978). Research has continued on this group of diverse taxa throughout the 20th and into the 21st century (Bradshaw & al. 1995; Schemske & Bradshaw 1999; Wu & al. 2008; Twyford & al. 2015; Yuan 2019), and Mimulus guttatus was one of the first non-model plants to be selected for full genome sequencing (Hellsten & al. 2013). Mimulus has played a key role in advancing our general understanding of the evolution of pollinator shifts (Bradshaw & Schemske 2003; Cooley & al. 2011; Byers & al. 2014), adaptation (Lowry & Willis 2010; Kooyers & al. 2015; Peterson & al. 2016; Ferris & Willis 2018; Troth & al. 2018), speciation (Ramsey & al. 2003; Wright & al. 2013; Sobel & Streisfeld 2015; Zuellig & Sweigart 2018), meiotic drive (Fishman & Saunders 2008), polyploidy (Vallejo-Marín 2012; Vallejo-Marín & al. 2015), range limits (Angert 2009; Sexton et al. 2011; Grossenbacher & al. 2014; Sheth & Angert 2014), circadian rhythms (Greenham & al. 2017), genetic recombination (Hellsten & al. 2013), mating systems (Fenster & Ritland 1994; Dudash & Carr 1998; Brandvain & al. 2014) and developmental biology (Moody & al. 1999; Baker & al. 2011, 2012; Yuan 2019). This combination of a rich history of study coupled with sustained modern research activity is unparalleled among angiosperms. Across many interested parties, the name Mimulus therefore takes on tremendous biological significance and is recognizable not only by botanists, but also by zoologists, horticulturalists, naturalists, and members of the biomedical community. Names associated with a taxonomic group of this prominence should have substantial inertia, and disruptive name changes should be avoided. As members of the Mimulus community, we advocate retaining the genus name Mimulus to describe all monkeyflowers. This is despite recent nomenclature changes that have led to a renaming of most monkeyflower species to other genera.Additional co-authors: Jannice Friedman, Dena L Grossenbacher, Liza M Holeski, Christopher T Ivey, Kathleen M Kay, Vanessa A Koelling, Nicholas J Kooyers, Courtney J Murren, Christopher D Muir, Thomas C Nelson, Megan L Peterson, Joshua R Puzey, Michael C Rotter, Jeffrey R Seemann, Jason P Sexton, Seema N Sheth, Matthew A Streisfeld, Andrea L Sweigart, Alex D Twyford, John H Willis, Kevin M Wright, Carrie A Wu, Yao-Wu Yua

Evolutionary convergence on hummingbird pollination in Neotropical Costus provides insight into the causes of pollinator shifts

The evolution of hummingbird pollination is common across angiosperms throughout the Americas, presenting an opportunity to examine convergence in both traits and environments to better understand how complex phenotypes arise. Here we examine independent shifts from bee to hummingbird pollination in the Neotropical spiral gingers (Costus) and address common explanations for the prevalence of transitions from bee to hummingbird pollination. We use floral traits of species with observed pollinators to predict pollinators of unobserved species and reconstruct ancestral pollination states on a well-resolved phylogeny. We examine whether independent transitions evolve towards the same phenotypic optimum and whether shifts to hummingbird pollination correlate with elevation or climate. Traits predicting hummingbird pollination include small flower size, brightly colored floral bracts and the absence of nectar guides. We find many shifts to hummingbird pollination and no reversals, a single shared phenotypic optimum across hummingbird flowers, and no association between pollination and elevation or climate. Evolutionary shifts to hummingbird pollination in Costus are highly convergent and directional, involve a surprising set of traits when compared with other plants with analogous transitions and refute the generality of several common explanations for the prevalence of transitions from bee to hummingbird pollination

Data from: The effect of range overlap on ecological niche divergence depends on spatial scale in monkeyflowers

Patterns of niche divergence and geographical range overlap of closely related species provide insights into the evolutionary dynamics of ecological niches. When ranges overlap, shared selective pressures may preserve niche similarity along coarse‐scale macrohabitat axes (e.g., bioclimates). Alternatively, competitive interactions may drive greater divergence along local‐scale microhabitat axes (e.g., micro‐topographical features). We tested these hypotheses in 16 species pairs of western North American monkeyflowers (Erythranthe and Diplacus, formerly Mimulus) with species’ niches, geographic ranges and a robust phylogeny. We found that macrohabitat niche divergence decreased with increasing range overlap, consistent with convergent selection operating at a coarse scale. No significant relationship was detected for microhabitat niches. Additionally, niche divergence was greater for young pairs along all macrohabitat niche axes, but greater for old pairs along one microhabitat axis related to vegetation cover. For a subset of species pairs with partially overlapping ranges, greater microhabitat divergence was detected in sympatry than in allopatry for at least one niche axis for three pairs, consistent with character displacement in sympatry. Thus, coarse‐ and local‐scale niche divergence show dissimilar patterns in relation to range overlap and evolutionary time, perhaps because the relative importance of convergent versus divergent selection depends on spatial scale

A geographic cline in the ability to self‐fertilize is unrelated to the pollination environment

The reproductive assurance (RA) hypothesis predicts that the ability to autonomously self‐fertilize should be favored in environments where a lack of mates or pollinators limits outcross reproduction. Because such limits to outcrossing are predicted to be most severe at range edges, elevated autonomy in peripheral populations is often attributed to RA. We test this hypothesis in 24 populations spanning the range of Campanula americana, including sampling at the range interior and three geographic range edges. We scored autonomous fruit set in a pollinator‐free environment and detected clinal variation—autonomy increased linearly from the southern to the northern edge, and from the eastern to the western edge. We then address whether the cline reflects the contemporary pollination environment. We measured population size, plant density, pollinator visitation, outcross pollen limitation and RA in natural populations over two years. Most populations were pollen limited, and those that experienced higher visitation rates by bumblebees had reduced pollen limitation. Reproductive assurance, however, was generally low across populations and was unrelated to pollen limitation or autonomy. Neither pollen limitation nor RA displayed geographic clines. Finally, autonomy was not associated with pollinator visitation rates or mate availability. Thus, the data do not support the RA hypothesis; clinal variation in autonomy is unrelated to the current pollination environment. Therefore, geographic patterns of autonomy are likely the result of historical processes rather than contemporary natural selection for RA

Data from: Impacts of worker density in colony-level aggression, expansion, and survival of the acacia-ant Crematogaster mimosae

Experimental studies assessing the impact of demographic changes on aggression and inter-group competitive outcomes in communities of social species are rare. This gap in our knowledge is important, not only because social species are foundational elements of many terrestrial ecosystems, but because interference competition among social groups often involves decision-like processes influenced by demographic and environmental contexts. In East Africa, the symbiotic ant Crematogaster mimosae is a co-dominant competitor that engages in high-mortality, intra- and interspecific battles for sole possession of host trees. We manipulated worker density on C. mimosae Acacia host trees, and the colony's opportunity to expand onto neighboring trees to identify how these factors influenced colony-level aggression, expansion success, and longer-term survivorship. Worker density on focal trees was increased through translocation of domatia-bearing branches, and was decreased using partial tree fumigations. We examined impacts of density manipulations on aggression and immediate expansion success under two different risk scenarios. We tied focal trees to either an experimentally emptied-tree (low-risk treatment), or to a C. nigriceps-occupied tree (high-risk treatment). Expansion success onto emptied neighbor trees was 100% for controls and increased-density colonies, but only 50% for decreased-density colonies, despite the fact that host trees are a limiting resource in this system. Success expanding onto trees occupied by a heterospecific competitor reached 36%, 40%, and 79% in decreased, control, and increased-density trees, respectively. Our results show that changes in worker density due to disturbances or inter-group battles have the potential to disrupt competitive hierarchies. Worker density manipulations also affected longer-term colony persistence. Behavioral and genetic data revealed that 12 months after expansions 100% of the decreased-density colonies, and 25% of control and increased-density colonies, had been supplanted by neighboring opportunistic conspecifics. Intraspecific aggression may have lower costs in C. mimosae because aggressive colonies can incorporate workers or queens from defeated competitors. The unexpectedly high frequency of conflicts between conspecific C. mimosae, in combination with behaviors decreasing the cost of intraspecific competition relative to interspecific conflict, may create opportunities for the survival of subordinate competitors in this ant–plant system

Self-compatibility is over-represented on islands

Because establishing a new population often depends critically on finding mates, individuals capable of uniparental reproduction may have a colonization advantage. Accordingly, there should be an over-representation of colonizing species in which individuals can reproduce without a mate, particularly in isolated locales such as oceanic islands. Despite the intuitive appeal of this colonization filter hypothesis (known as Baker's law), more than six decades of analyses have yielded mixed findings. We assembled a dataset of island and mainland plant breeding systems, focusing on the presence or absence of self-incompatibility. Because this trait enforces outcrossing and is unlikely to re-evolve on short timescales if it is lost, breeding system is especially likely to reflect the colonization filter. We found significantly more self-compatible species on islands than mainlands across a sample of > 1500 species from three widely distributed flowering plant families (Asteraceae, Brassicaceae and Solanaceae). Overall, 66% of island species were self-compatible, compared with 41% of mainland species. Our results demonstrate that the presence or absence of self-incompatibility has strong explanatory power for plant geographical patterns. Island floras around the world thus reflect the role of a key reproductive trait in filtering potential colonizing species in these three plant families