The genetic basis of traits associated with the evolution of serpentine endemism in monkeyflowers.

The floras on chemically and physically challenging soils, such as gypsum, shale, and serpentine, are characterized by narrowly endemic species. The evolution of edaphic endemics may be facilitated or constrained by genetic correlations among traits contributing to adaptation and reproductive isolation across soil boundaries. The yellow monkeyflowers in the Mimulus guttatus species complex are an ideal system in which to examine these evolutionary patterns. To determine the genetic basis of adaptive and prezygotic isolating traits, we performed genetic mapping experiments with F2 hybrids derived from a cross between a serpentine endemic, M. nudatus, and its close relative M. guttatus. Few large effect and many small effect QTL contribute to interspecific divergence in life history, floral, and leaf traits, and a history of directional selection contributed to trait divergence. Loci contributing to adaptive traits and prezygotic reproductive isolation overlap, and their allelic effects are largely in the direction of species divergence. These loci contain promising candidate genes regulating flowering time and plant organ size. Together, our results suggest that genetic correlations among traits can facilitate the evolution of adaptation and speciation and may be a common feature of the genetic architecture of divergence between edaphic endemics and their widespread relatives.

An evolutionary framework for understanding habitat partitioning in plants.

Many plant species with overlapping geographic ranges segregate at smaller spatial scales. This spatial segregation-zonation when it follows an abiotic gradient and habitat partitioning when it does not-has been experimentally investigated for over a century often using distantly related taxa, such as different genera of algae or barnacles. In those foundational studies, trade-offs between stress tolerance and competitive ability were found to be the major driving factors of habitat partitioning for both animals and plants. Yet, the evolutionary relationships among segregating species are usually not taken into account. Since close relatives are hypothesized to compete more intensely and are more likely to interact during mating compared to distant relatives, the mechanisms underlying habitat partitioning may differ depending on the relatedness of the species in question. Here, I propose an integration of ecological and evolutionary factors contributing to habitat partitioning in plants, specifically how the relative contributions of factors predictably change with relatedness of taxa. Interspecific reproductive interactions in particular are understudied, yet important drivers of habitat partitioning. In spatially segregated species, interspecific mating can reduce the fitness of rare immigrants, preventing their establishment and maintaining patterns of spatial segregation. In this synthesis, I review the literature on mechanisms of habitat partitioning in plants within an evolutionary framework, identifying knowledge gaps and detailing future directions for this rapidly growing field of study.

Frequency-Dependent Hybridization Contributes to Habitat Segregation in Monkeyflowers.

AbstractSpatial segregation of closely related species is usually attributed to differences in stress tolerance and competitive ability. For both animals and plants, reproductive interactions between close relatives can impose a fitness cost that is more detrimental to the rarer species. Frequency-dependent mating interactions may thus prevent the establishment of immigrants within heterospecific populations, maintaining spatial segregation of species. Despite strong spatial segregation in natural populations, two sympatric California monkeyflowers (Mimulus nudatus and M. guttatus) survive and reproduce in the other's habitat when transplanted reciprocally. We hypothesized that a frequency-dependent mating disadvantage maintains spatial segregation of these monkeyflowers during natural immigration. To evaluate this hypothesis, we performed two field experiments. First, we experimentally added immigrants in varying numbers to sites dominated by heterospecifics. Second, we reciprocally transplanted arrays of varying resident and immigrant frequencies. Immigrant seed viability decreased with conspecific rarity for M. guttatus but not for M. nudatus. We observed immigrant minority disadvantage for both species, but it was driven by different factors-frequency-dependent hybridization for M. guttatus and competition for resources and/or pollinators for M. nudatus. Overall, our results suggest a major role for reproductive interference in spatial segregation that should be evaluated along with stress tolerance and competitive ability.

Inbreeding depression contributes to the maintenance of habitat segregation between closely related monkeyflower species.

Incompletely reproductively isolated species often segregate into different microhabitats, even when they are able to survive and reproduce in both habitats. Longer term evolutionary factors may contribute to this lack of cross-habitat persistence. When reproductive interference reduces immigrant fitness, assortative mating, including self-fertilization, increases immigrants' fitness in a single generation, but longer term, inbreeding depression may reduce the chance of population persistence. Two California monkeyflower species repeatedly segregate into drier and wetter areas in their zone of sympatry. To test whether inbreeding depression may contribute to the maintenance of this segregation pattern, we transplanted outbred and successively inbred Mimulus guttatus and Mimulus nudatus into their native habitats and heterospecific habitats. We measured germination, survival, and seed set and found that recurrent selfing reduced all aspects of fitness in both species, most strongly in foreign habitats. A simulation model, parameterized from the transplant experiment, found that inbreeding reduced fitness to such an extent that sequentially inbred populations of either species would be unable to persist in heterospecific-occupied habitats in the absence of continued gene flow. These results demonstrate that individual immigrants are unlikely to form persistent populations and thus, inbreeding depression contributes to the absence of fine-scale coexistence in this species pair.

Hybrid inviability and differential submergence tolerance drive habitat segregation between two congeneric monkeyflowers.

Closely related, ecologically similar species are often separated at small geographic scales while being broadly sympatric. Both adaptation to abiotic environmental conditions and a variety of biotic interactions may determine small-scale allopatry. In Northern California's coast range, two monkeyflower species, Mimulus guttatus and Mimulus nudatus, can co-occur within local sites but rarely overlap at fine spatial scales, even though they are often separated by less than 1 m. M. guttatus naturally grows in wetter areas and is often submerged for up to four months of the year, while M. nudatus naturally occupies drier sites. We used a combination of observational data, reciprocal transplant, and laboratory experiments to test a series of biotic and abiotic hypotheses for the observed distribution pattern. Although M. guttatus can tolerate dry hillside conditions like those in which M. nudatus occurs, M. nudatus is unable to survive submerged for more than a week, limiting its distribution from seasonal streams inundated for months and dominated by M. guttatus. While herbivores did not differentially damage species, transplants were more likely to be damaged in M. guttatus' seep habitat and M. nudatus was less tolerant to herbivory. Individuals of each species transplanted into populations of heterospecific congeners produced large proportions (up to 80%) of inviable seeds resulting from increased hybridization rates in close sympatry. Mimulus nudatus' inability to tolerate submergence and herbivory establishes some degree of habitat association, and then, hybrid seed inviability reduces the ability of the locally rarer species to persist within the congener's microhabitat and maintains habitat segregation. Together these data show that both environmental filtering and biotic interactions shape the fine-scale distribution of close relatives.

Effects of wildfire on floral display size and pollinator community reduce outcrossing rate in a plant with a mixed mating system.

PREMISE OF THE STUDY: Wildfire changes the demography, morphology, and behavior of plants, and may alter the pollinator community. Such trait changes may drastically alter the outcome of pollination mutualisms on plants; however, the direct role of fire on these mutualisms is poorly known. METHODS: Following a pair of fires in the northern California coast range chaparral, we censused floral visitor communities of Trichostema laxum (Lamiaceae), quantified visiting bee behavior, and estimated outcrossing rates using a widespread Mendelian recessive floral polymorphism across a matrix of populations in burned and unburned sites. We also compared pre- and postfire floral visitation in two populations. RESULTS: Outcrossing rates were significantly lower in burned areas; however, our data suggest that the much larger size of plants in burned areas, not burn status itself, drove this pattern. Large-bodied bees dominated floral visitor communities after fire, likely recruiting to the abundant postfire floral resources. These bees visited more flowers per plant than did the smaller bees prevalent before fire and in unburned areas, likely increasing selfing through geitonogamy (within-plant pollination), an effect made possible by the far larger size of plants in burned areas. CONCLUSIONS: Outcrossing rates dropped substantially after wildfires because of changes in the pollinators, plant display size, and their interactions. Reductions in outcrossing following fire may have important implications for population resilience and evolution in a changing climate with more frequent fires.

Leaf shape evolution has a similar genetic architecture in three edaphic specialists within the Mimulus guttatus species complex.

BACKGROUND AND AIMS: The genetic basis of leaf shape has long interested botanists because leaf shape varies extensively across the plant kingdom and this variation is probably adaptive. However, knowledge of the genetic architecture of leaf shape variation in natural populations remains limited. This study examined the genetic architecture of leaf shape diversification among three edaphic specialists in the Mimulus guttatus species complex. Lobed and narrow leaves have evolved from the entire, round leaves of M. guttatus in M. laciniatus, M. nudatus and a polymorphic serpentine M. guttatus population (M2L). METHODS: Bulk segregant analysis and next-generation sequencing were used to map quantitative trait loci (QTLs) that underlie leaf shape in an M. laciniatus × M. guttatus F2 population. To determine whether the same QTLs contribute to leaf shape variation in M. nudatus and M2L, F2s from M. guttatus × M. nudatus and lobed M2L × unlobed M. guttatus crosses were genotyped at QTLs from the bulk segregant analysis. KEY RESULTS: Narrow and lobed leaf shapes in M. laciniatus, M. nudatus and M. guttatus are controlled by overlapping genetic regions. Several promising leaf shape candidate genes were found under each QTL. CONCLUSIONS: The evolution of divergent leaf shape has taken place multiple times in the M. guttatus species complex and is associated with the occupation of dry, rocky environments. The genetic architecture of elongated and lobed leaves is similar across three species in this group. This may indicate that parallel genetic evolution from standing variation or new mutations is responsible for the putatively adaptive leaf shape variation in Mimulus.