David C. Haak

Impacts of climate warming on terrestrial ectotherms across latitude

The impact of anthropogenic climate change on terrestrial organisms is often predicted to increase with latitude, in parallel with the rate of warming. Yet the biological impact of rising temperatures also depends on the physiological sensitivity of organisms to temperature change. We integrate empirical fitness curves describing the thermal tolerance of terrestrial insects from around the world with the projected geographic distribution of climate change for the next century to estimate the direct impact of warming on insect fitness across latitude. The results show that warming in the tropics, although relatively small in magnitude, is likely to have the most deleterious consequences because tropical insects are relatively sensitive to temperature change and are currently living very close to their optimal temperature. In contrast, species at higher latitudes have broader thermal tolerance and are living in climates that are currently cooler than their physiological optima, so that warming may even enhance their fitness. Available thermal tolerance data for several vertebrate taxa exhibit similar patterns, suggesting that these results are general for terrestrial ectotherms. Our analyses imply that, in the absence of ameliorating factors such as migration and adaptation, the greatest extinction risks from global warming may be in the tropics, where biological diversity is also greatest.

Increased structure and active learning reduce the achievement gap in introductory biology.

A focus on problem-solving skills reduced achievement gaps in university classes. Science, technology, engineering, and mathematics instructors have been charged with improving the performance and retention of students from diverse backgrounds. To date, programs that close the achievement gap between students from disadvantaged versus nondisadvantaged educational backgrounds have required extensive extramural funding. We show that a highly structured course design, based on daily and weekly practice with problem-solving, data analysis, and other higher-order cognitive skills, improved the performance of all students in a college-level introductory biology class and reduced the achievement gap between disadvantaged and nondisadvantaged students—without increased expenditures. These results support the Carnegie Hall hypothesis: Intensive practice, via active-learning exercises, has a disproportionate benefit for capable but poorly prepared students.

Increased Course Structure Improves Performance in Introductory Biology

We tested the hypothesis that highly structured course designs, which implement reading quizzes and/or extensive in-class active-learning activities and weekly practice exams, can lower failure rates in an introductory biology course for majors, compared with low-structure course designs that are based on lecturing and a few high-risk assessments. We controlled for 1) instructor effects by analyzing data from quarters when the same instructor taught the course, 2) exam equivalence with new assessments called the Weighted Blooms Index and Predicted Exam Score, and 3) student equivalence using a regression-based Predicted Grade. We also tested the hypothesis that points from reading quizzes, clicker questions, and other “practice” assessments in highly structured courses inflate grades and confound comparisons with low-structure course designs. We found no evidence that points from active-learning exercises inflate grades or reduce the impact of exams on final grades. When we controlled for variation in student ability, failure rates were lower in a moderately structured course design and were dramatically lower in a highly structured course design. This result supports the hypothesis that active-learning exercises can make students more skilled learners and help bridge the gap between poorly prepared students and their better-prepared peers.

Evolutionary ecology of pungency in wild chilies.

The primary function of fruit is to attract animals that disperse viable seeds, but the nutritional rewards that attract beneficial consumers also attract consumers that kill seeds instead of dispersing them. Many of these unwanted consumers are microbes, and microbial defense is commonly invoked to explain the bitter, distasteful, occasionally toxic chemicals found in many ripe fruits. This explanation has been criticized, however, due to a lack of evidence that microbial consumers influence fruit chemistry in wild populations. In the present study, we use wild chilies to show that chemical defense of ripe fruit reflects variation in the risk of microbial attack. Capsaicinoids are the chemicals responsible for the well known pungency of chili fruits. Capsicum chacoense is naturally polymorphic for the production of capsaicinoids and displays geographic variation in the proportion of individual plants in a population that produce capsaicinoids. We show that this variation is directly linked to variation in the damage caused by a fungal pathogen of chili seeds. We find that Fusarium fungus is the primary cause of predispersal chili seed mortality, and we experimentally demonstrate that capsaicinoids protect chili seeds from Fusarium. Further, foraging by hemipteran insects facilitates the entry of Fusarium into fruits, and we show that variation in hemipteran foraging pressure among chili populations predicts the proportion of plants in a population producing capsaicinoids. These results suggest that the pungency in chilies may be an adaptive response to selection by a microbial pathogen, supporting the influence of microbial consumers on fruit chemistry.

Costs and benefits of capsaicin-mediated control of gut retention in dispersers of wild chilies

A fundamental way in which animal-dispersed plants can influence the viability and distribution of dispersed seeds is through control of retention time in the guts of dispersers. Using two species of wild chilies and their dispersers, we examined how chemical and physical properties of fruits and seeds mediate this interaction. Capsicum chacoense is polymorphic for pungency, occurs in Bolivia, and is dispersed mostly by elaenias. Capsicum annuum is not polymorphic, occurs in Arizona (USA), and is dispersed mostly by thrashers. We first tested whether capsaicin, the substance responsible for the pungency of chilies, affects gut retention time of seeds in primary dispersers. Capsaicin slowed gut passage of seeds but did so in a manner that differed greatly between bird species because the constipative effects of capsaicin occurred only after an 80-minute time lag. Elaenias in Bolivia held only 6% of C. chacoense seeds for > 80 minutes, whereas thrashers in Arizona held 78% of C. annuum seeds for > 80 minutes. Next we examined the effects of retention time on seed viability and germination. Increased retention resulted in a greater proportion of seeds germinating in C. annuum, had no effects on non-pungent C. chacoense, and had negative effects on pungent C. chacoense. These divergent effects are explained by differences in seed coat morphology: seed coats of pungent C. chacoense are 10-12% thinner than those of the other two types of seeds. Thus, longer retention times damaged seeds with the thinnest seed coats. In C. annuum, seed viability remained high regardless of retention time, but germination increased with retention, suggesting a role for scarification. Thus, in C. annuum, fruit chemistry appears well matched with seed morphology and disperser physiology: capsaicin extends gut retention for most seeds, resulting in greater seed scarification and higher germination rates. Increased retention of pungent C. chacoense seeds is detrimental, but because the primary consumers have short retention times, capsaicin slows only a small proportion of seeds, minimizing negative effects. These results illustrate the importance of context in studies of fruit secondary metabolites. The same chemical can have different impacts on plant fitness depending on its morphological, physiological, and ecological context.

No evidence for phylogenetic constraint on natural defense evolution among wild tomatoes

Plant defense traits can be shaped by evolutionary and physiological constraints, as well as local ecological selection. We assessed the relative importance of these factors in shaping defense trait variation across the wild tomato clade (a group of 13 closely related species) using an herbivore bioassay (Manduca sexta). With phylogenetic comparative methods, we evaluated patterns of constitutive and induced defense variation, and the extent of coupling between alternative defense strategies. We detected substantial variation among species and found no evidence for phylogenetic conservatism among defensive traits, unlike for two other ecologically relevant (reproductive) traits. In addition, constitutive and induced defense syndromes were unassociated. These data indicate that, in this group, there is no evidence for either phylogenetic conservatism of shared consumer guilds that shape defense traits, or for constraints on defense trait evolution, including mechanistic trade-offs between defense strategies. Our data suggest that defense trait variation in this clade instead results from rapid responses to local ecological conditions.

Why are not all chilies hot? A trade-off limits pungency

Evolutionary biologists increasingly recognize that evolution can be constrained by trade-offs, yet our understanding of how and when such constraints are manifested and whether they restrict adaptive divergence in populations remains limited. Here, we show that spatial heterogeneity in moisture maintains a polymorphism for pungency (heat) among natural populations of wild chilies (Capsicum chacoense) because traits influencing water-use efficiency are functionally integrated with traits controlling pungency (the production of capsaicinoids). Pungent and non-pungent chilies occur along a cline in moisture that spans their native range in Bolivia, and the proportion of pungent plants in populations increases with greater moisture availability. In high moisture environments, pungency is beneficial because capsaicinoids protect the fruit from pathogenic fungi, and is not costly because pungent and non-pungent chilies grown in well-watered conditions produce equal numbers of seeds. In low moisture environments, pungency is less beneficial as the risk of fungal infection is lower, and carries a significant cost because, under drought stress, seed production in pungent chilies is reduced by 50 per cent relative to non-pungent plants grown in identical conditions. This large difference in seed production under water-stressed (WS) conditions explains the existence of populations dominated by non-pungent plants, and appears to result from a genetic correlation between pungency and stomatal density: non-pungent plants, segregating from intra-population crosses, exhibit significantly lower stomatal density (p = 0.003), thereby reducing gas exchange under WS conditions. These results demonstrate the importance of trait integration in constraining adaptive divergence among populations.