Determinants of geographic distribution in western North American monkeyflowers

2014 Summer.The geographic range of a species represents the basic unit of biogeography. Despite ample evidence that properties of geographic ranges vary among species, we do not fully understand the ecological and evolutionary processes underlying these patterns, thereby hindering our ability to forecast changes in species' distributions in response to changing environments. Key hypotheses about variation in geographic range size among species emphasize the roles of ecological niche properties and the connectivity of suitable habitat. In the first study of my dissertation, I combined primary occurrence data with climate variables to test the relative importance of these hypotheses in 72 species of western North American monkeyflower (genus Mimulus). Climatic niche breadth, via its effect on the amount of suitable habitat, was a strong predictor of geographic range size, whereas climatic niche position (relative to regional climate) and connectivity of climatically suitable habitat were not. Given the role of climatic niche breadth in shaping geographic range sizes in Mimulus, the goal of the second study of my dissertation was to examine the relationship between thermal tolerance (an important axis of niche breadth) and range size experimentally using 5 pairs of closely related Mimulus species with differing range sizes. Within four species pairs, the more geographically widespread species had a broader thermal tolerance than the narrowly distributed species, providing further support for the hypothesis that species with broader niches are able to achieve larger geographic ranges. Further, within each species pair, the species with broader thermal tolerance encompassed greater variation in temperature across its geographic range and higher genetic variation for thermal tolerance than the species with narrower thermal tolerance, supporting the hypotheses that climatic variability and genetic variation in ecologically important traits can explain variation in environmental tolerance among species. Although species vary in range size, every species has a limited geographic range, leading to the question of what prevents a species from expanding its range via niche evolution. Thus, in the third study of my dissertation, I tested whether adaptation at geographic range margins is constrained by insufficient evolutionary potential. To do so, I used artificial selection experiments to quantify genetic variation in flowering time for populations from the northern edge, center, and southern edge of the geographic range of the scarlet monkeyflower (M. cardinalis). Contrary to prediction, southern populations exhibited significantly greater responses to selection (and thus evolutionary potential) than northern or central populations. Together, these results highlight an important role of niche breadth in explaining variation in geographic range size among species, and reveal variation in evolutionary potential that facilitates niche and range expansion within and among species

PATTERNS OF HABITAT USE BY PRIMATES IN EASTERN ECUADOR

Lowland tropical rain forests of western Amazonia are characterized by the most speciose primate communities in the Neotropics, immediately leading to the question of to what extent does niche partitioning by primate species serve as a mechanism to promote species co-existence. Because the primate assemblages that we observe today reflect a combination of ecological and evolutionary processes, this study examines habitat occupancy and its relationship to phylogeny and space in a diverse diurnal primate community in an undisturbed lowland rain forest of Amazonian Ecuador. Specifically, the following null hypotheses are explored as potential factors that shape community structure: (1) mean height in the forest strata does not differ among species; (2) species occupy habitat types at frequencies proportional to their overall availability; (3) species do not segregate in ecological space; (4) there is no relationship between phylogenetic distance and ecological distance among species; and (5) there is no relationship between ecological distance and geographic distance among species. The results of this study reveal that ecological differences among the species in this primate community facilitate their coexistence. Larger species generally occupied higher strata than smaller ones. Furthermore, although they generally tended to occupy habitat types at frequencies proportional to their availability in the study area, species segregated in ecological space defined by dissimilarity in habitat occupancy. Finally, in this community, a clear relationship was not observed between phylogenetic and ecological distances or ecological and geographic distances. This study elucidates the spatial distribution and the habitat partitioning of the diurnal primate community at the Tiputini Biodiversity Station in Ecuadorian Amazonia

Quantifying the Impact of Gene Flow on Phenotype-Environment Mismatch: A Demonstration with the Scarlet Monkeyflower Mimulus cardinalis

Geographic range margins offer testing grounds for limits to adaptation. If range limits are concordant with niche limits, range expansions require the evolution of new phenotypes that can maintain populations beyond current range margins. However, many species\u27 range margins appear static over time, suggesting limits on the ability of marginal populations to evolve appropriate phenotypes. A potential explanation is the swamping gene flow hypothesis, which posits that asymmetrical gene flow from large, well-adapted central populations prevents marginal populations from locally adapting. We present an empirical framework for combining gene flow, environment, and fitness-related phenotypes to infer the potential for maladaptation, and we demonstrate its application using the scarlet monkeyflower Mimulus cardinalis. We grew individuals sampled from populations on a latitudinal transect under varied temperatures and determined the phenotypic deviation (PD), the mismatch between phenotype and local environment. We inferred gene flow among populations and predicted that populations receiving the most temperature- or latitude-weighted immigration would show the greatest PD and that these populations were likely marginal. We found asymmetrical gene flow from central to marginal populations. Populations with more latitude-weighted immigration had significantly greater PD but were not necessarily marginal. Gene flow may limit local adaptation in this species, but swamping gene flow is unlikely to explain its northern range limit

The evolution of thermal performance in native and invasive populations of Mimulus guttatus

The rise of globalization has spread organisms beyond their natural range, allowing further opportunity for species to adapt to novel environments and potentially become invaders. Yet, the role of thermal niche evolution in promoting the success of invasive species remains poorly understood. Here, we use thermal performance curves (TPCs) to test hypotheses about thermal adaptation during the invasion process. First, we tested the hypothesis that if species largely conserve their thermal niche in the introduced range, invasive populations may not evolve distinct TPCs relative to native populations, against the alternative hypothesis that thermal niche and therefore TPC evolution has occurred in the invasive range. Second, we tested the hypothesis that clines of TPC parameters are shallower or absent in the invasive range, against the alternative hypothesis that with sufficient time, standing genetic variation, and temperature-mediated selection, invasive populations would re-establish clines found in the native range in response to temperature gradients. To test these hypotheses, we built TPCs for 18 native (United States) and 13 invasive (United Kingdom) populations of the yellow monkeyflower, Mimulus guttatus. We grew clones of multiple genotypes per population at six temperature regimes in growth chambers. We found that invasive populations have not evolved different thermal optima or performance breadths, providing evidence for evolutionary stasis of thermal performance between the native and invasive ranges after over 200 years post introduction. Thermal optimum increased with mean annual temperature in the native range, indicating some adaptive differentiation among native populations that was absent in the invasive range. Further, native and invasive populations did not exhibit adaptive clines in thermal performance breadth with latitude or temperature seasonality. These findings suggest that TPCs remained unaltered post invasion, and that invasion may proceed via broad thermal tolerance and establishment in already climatically suitable areas rather than rapid evolution upon introduction

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

Effect of fragment size on non-volant mammals in La Cruz and Monteverde, Costa Rica

The purpose of this study was to examine the effects of fragment size on terrestrial, fruit-eating mammals. In this study, it was expected that there would be smaller mammals in small fragments than in large ones due to limited resources and fewer predators. In each of five fragments of different sizes and in a section of continuous forest, plantains were used to bait mammals, and each site was checked every other day for damage to bait. Based on observations of bite marks on plantains, for groups of mammals were identified: small rodents, opossums, agoutis and pacas, and coatis. Number of total visits to bait tended to decrease with increasing fragment size. Proportions of visits by small rodents were higher in smaller fragments. There was no significant difference between number of visits between fragments and continuous forest (Friedman test, p = 0.2409), but there was a significant difference between the different types of damage to bait in the six study sites (Friedman test, p = 0.0014). Specifically, multiple comparisons indicate that the number of plantains not found at the study sites (presumably because they were removed by larger mammals) was significantly higher than the number of visits by opossums (p \u3c 0.05). These results suggest that fragmentation can influence relative abundances of fruit-eating mammals, which can be seed dispersers crucial to seedling recruitment. En este estudio, se examinó los efectos de la fragmentación del bosque en los mamíferos terrestres que comen frutas. Se predijo que habría más mamíferos pequeños en fragmentos menores que en los fragmentos grandes, a causa de lo limitado de los recursos y menos predadores. En cada uno de los cinco fragmentos de diferentes tamaños y en una sección del bosque continuo, plátanos fueron usados para atraer los mamíferos y cada lugar fue inspeccionado cada dos días. Basado en observaciones de las marcas de dientes en los plátanos, cuatro grupos de mamíferos fueron identificados: los roedores pequeños, los zorros, las guatusas y tepezcuintles, y los pizotes. El número de visitas totales al cebo disminuyo con el aumento en el tamaño del fragmento. Proporciones de visitas por los roedores pequeños fueron mas altas en fragmentos pequeños que en fragmentos grandes. No había una diferencia significativa entre el número de visitas entre los fragmentos y el bosque continuo (prueba Friedman, p = 0.2409), pero había una diferencia significativa entre los diferentes tipos de daño al cebo en los lugares del estudio (prueba Friedman, p = 0.0014). Específicamente, las pruebas posteriores (Post-hoc test) indicaron que le número de plátanos no encontrados (porque los mamíferos mas grandes los removieron) en los lugares del estudio, fue de manera significativa mayor que el de las visitas por los zorros. Estos resultados sugieren que la fragmentación puede influir las abundancias relativas de los mamíferos que comen fruta. Estos mamíferos son importantes para la dispersión de semillas y por eso, son cruciales para la sucesión de muchas plantas.https://digitalcommons.usf.edu/tropical_ecology/1224/thumbnail.jp

Effect of fragment size on non-volant mammals in La Cruz and Monteverde, Costa Rica

The purpose of this study was to examine the effects of fragment size on terrestrial, fruit-eating mammals. In this study, it was expected that there would be smaller mammals in small fragments than in large ones due to limited resources and fewer predators. In each of five fragments of different sizes and in a section of continuous forest, plantains were used to bait mammals, and each site was checked every other day for damage to bait. Based on observations of bite marks on plantains, for groups of mammals were identified: small rodents, opossums, agoutis and pacas, and coatis. Number of total visits to bait tended to decrease with increasing fragment size. Proportions of visits by small rodents were higher in smaller fragments. There was no significant difference between number of visits between fragments and continuous forest (Friedman test, p = 0.2409), but there was a significant difference between the different types of damage to bait in the six study sites (Friedman test, p = 0.0014). Specifically, multiple comparisons indicate that the number of plantains not found at the study sites (presumably because they were removed by larger mammals) was significantly higher than the number of visits by opossums (p \u3c 0.05). These results suggest that fragmentation can influence relative abundances of fruit-eating mammals, which can be seed dispersers crucial to seedling recruitment. En este estudio, se examinó los efectos de la fragmentación del bosque en los mamíferos terrestres que comen frutas. Se predijo que habría más mamíferos pequeños en fragmentos menores que en los fragmentos grandes, a causa de lo limitado de los recursos y menos predadores. En cada uno de los cinco fragmentos de diferentes tamaños y en una sección del bosque continuo, plátanos fueron usados para atraer los mamíferos y cada lugar fue inspeccionado cada dos días. Basado en observaciones de las marcas de dientes en los plátanos, cuatro grupos de mamíferos fueron identificados: los roedores pequeños, los zorros, las guatusas y tepezcuintles, y los pizotes. El número de visitas totales al cebo disminuyo con el aumento en el tamaño del fragmento. Proporciones de visitas por los roedores pequeños fueron mas altas en fragmentos pequeños que en fragmentos grandes. No había una diferencia significativa entre el número de visitas entre los fragmentos y el bosque continuo (prueba Friedman, p = 0.2409), pero había una diferencia significativa entre los diferentes tipos de daño al cebo en los lugares del estudio (prueba Friedman, p = 0.0014). Específicamente, las pruebas posteriores (Post-hoc test) indicaron que le número de plátanos no encontrados (porque los mamíferos mas grandes los removieron) en los lugares del estudio, fue de manera significativa mayor que el de las visitas por los zorros. Estos resultados sugieren que la fragmentación puede influir las abundancias relativas de los mamíferos que comen fruta. Estos mamíferos son importantes para la dispersión de semillas y por eso, son cruciales para la sucesión de muchas plantas.https://digitalcommons.usf.edu/tropical_ecology/1224/thumbnail.jp

Data from: Demographic compensation does not rescue populations at a trailing range edge

Species' geographic ranges and climatic niches are likely to be increasingly mismatched due to rapid climate change. If a species' range and niche are out of equilibrium, then population performance should decrease from high-latitude "leading" range edges, where populations are expanding into recently ameliorated habitats, to low-latitude "trailing" range edges, where populations are contracting from newly unsuitable areas. Demographic compensation is a phenomenon whereby declines in some vital rates are offset by increases in others across time or space. In theory, demographic compensation could increase the range of environments over which populations can succeed and forestall range contraction at trailing edges. An outstanding question is whether range limits and range contractions reflect inadequate demographic compensation across environmental gradients, causing population declines at range edges. We collected demographic data from 32 populations of the scarlet monkeyflower (Erythranthe cardinalis) spanning 11˚ latitude in western North America and used integral projection models to evaluate population dynamics and assess demographic compensation across the species' range. During the 5-year study period, which included multiple years of severe drought and warming, population growth rates decreased from north to south, consistent with leading-trailing dynamics. Southern populations at the trailing range edge declined due to reduced survival, growth, and recruitment, despite compensatory increases in reproduction and faster life history characteristics. These results suggest that demographic compensation may only delay population collapse without the return of more favorable conditions or the contribution of other buffering mechanisms such as evolutionary rescue

Data from: Artificial selection reveals high genetic variation in phenology at the trailing edge of a species range

Species' responses to climate change depend on the interplay of migration and adaptation, yet we know relatively little about the potential for adaptation. Genetic adaptations to climate change often involve shifts in the timing of phenological events such as flowering. If populations at the edge of a species' range have lower genetic variation in phenological traits than central populations, then their persistence under climate change could be threatened. To test this hypothesis, we performed artificial selection experiments using the scarlet monkeyflower (Mimulus cardinalis) and compared genetic variation in flowering time among populations at the latitudinal center, northern edge, and southern edge of the species' range. We also assessed whether selection on flowering time yielded correlated responses in functional traits, potentially representing a cost associated with early or late flowering. Contrary to prediction, southern populations exhibited greater responses to selection on flowering time than central or northern populations. Further, selection for early flowering resulted in correlated increases in specific leaf area and leaf nitrogen, whereas selection for late flowering led to decreases in these traits. These results provide critical insights about how spatial variation in the potential for adaptation may affect population persistence under changing climates