Christina Caruso

Multi-level selection and the evolution of gynodioecy

• Gynodioecy is a sexual polymorphism where female plants and hermaphroditic plants coexist within populations. Although <1% of flowering plant species are gynodioecious, gynodioecy has repeatedly evolved: gynodioecious species are found in 91 families across 36 orders (Caruso et al. 2016), and within some of these families gynodioecy has independently evolved multiple times (Rivkin et al. 2016).
• Gynodioecy is evolutionarily labile; lineages in which gynodioecy has frequently evolved also have a high rate of reversions to hermaphroditism (Rivkin et al. 2016).
• Gynodioecy is maintained in part because females produce more seeds when they are rare than when they are common (i.e. frequency-dependent selection; Rivkin et al. 2015). We hypothesize that females can detect whether they are rare or common by eavesdropping on the floral volatiles emitted by their hermaphroditic neighbors (Caruso and Parachnowitsch 2016).
• ​Gynodioecy is maintained in part because hermaphrodites that carry a mismatched sex-determining allele have lower pollen viability than hermaphrodites that do not carry a mismatched allele (i.e. gametic selection against the spread of nuclear fertility restorer alleles; Case and Caruso 2010; Caruso et al. 2012). This selection can explain why females plants are common in some populations, but rare in others (Caruso and Case 2007, 2013).
• Although females are more common in populations where annual mean temperature is higher (Caruso and Case 2007), temperature does not affect selection on female plants; neither the seed fertility of females relative to hermaphrodites nor the pollen viability of hermaphrodites differed between high- and low-temperature treatments (Bailey et al. 2017). 

Evolution of photosynthetic and stomatal traits

• Plants respond to variation in soil water availability by plastically adjusting leaf-level photosynthetic and stomatal traits. This plasticity is adaptive in some species, but not in others (Maherali et al. 2010; Caruso et al. 2006).
• Plasticity in leaf-level photosynthetic and stomatal traits is not costly (Maherali et al. 2010; Caruso et al. 2006).
• ​The evolution of photosynthetic and stomatal traits may be limited by a lack of genetic variation rather than by natural selection against unfit trait combinations  (Caruso et al. 2005; Donovan et al. 2011; Caruso and Maherali, unpublished).

The causes of natural selection

• Selection on floral traits can be caused by pollinators, even when reproduction is not pollen-limited (Caruso et al. 2010).
• Not all selection on floral traits is caused by pollinators. Selection on floral traits can also be caused by insect seed predators (Parachnowitsch and Caruso 2008; Caruso et al. 2010), mammalian browsers (Walsh and Caruso, unpublished), soil water and nutrients (Caruso et al. 2005), competitors for pollination (Caruso 1999), and predators of pollinators (Benoit and Caruso, unpublished)..
• ​Precipitation is an important cause of temporal and spatial variation in selection at a global scale (Siepielski et al. 2017 and in press).
• Biotic environmental factors are not a more important cause of selection than abiotic environmental factors. However, the effects of biotic and abiotic environmental factors on selection can be predicted from their effects on mean fitness (Caruso et al. 2017).   

The effect of human-mediated environmental change on natural selection

• Declines in pollinator populations can intensify natural selection on attractive floral traits (Brown and Caruso, unpublished).

• Caruso, C. M., R. A. Martin, N. Sletvold, M. B. Morrissey, M. J. Wade, K. E. Augustine, S. M. Carlson, A. D. C. MacColl, A. M. Siepielski, and J. G. Kingsolver. 2017. What are the environmental determinants of phenotypic selection? A meta-analysis of experimental studies. The American Naturalist 190: 363-376.
• Bailey. M. F., A. L. Case, and C. M. Caruso. 2017. Physiological effects of temperature do not explain prevalence of females in populations of gynodioecious Lobelia siphilitica growing in warmer climates. American Journal of Botany 104: 411-418.
• Siepielski, A., M. B. Morrissey, M. Buoro, S. M. Carlson, C. M. Caruso, S. M. Clegg, T. Coulson, J. Di Battista, K. M. Gotanda, C. D. Francis, J. Hereford, J. G. Kingsolver, K. E. Augustine, L. E. B. Kruuk, R. A. Martin, B. C. Sheldon, N. Sletvold, E. I. Svensson, M. J. Wade, and A. D. C. MacColl. 2017. Precipitation drives global variation in natural selection. Science 355: 959-962.
• Eisen, K., A. L. Case, and C. M. Caruso. 2017. Variation in pollen dispensing schedules of Lobelia siphilitica. International Journal of Plant Sciences 178: 79-84.
• Rivkin, L. R., A. L. Case, and C. M. Caruso. 2016. Why is gynodioecy a rare but widely distributed sexual system? Lessons from the Lamiaceae. New Phytologist 211: 688-696.
• Caruso, C. M., K. Eisen, and A. L. Case. 2016. An angiosperm-wide analysis of the correlates of gynodioecy. International Journal of Plant Sciences 177: 115-121.
• Caruso, C. M. and A. L. Parachnowitsch. 2016. Do plants eavesdrop in floral scent signals? Trends in Plant Science 21: 9-15.

• BIOL*3010 - Laboratory and Fieldwork in Ecology (Fall 2024)

• Ariana Longley (MSc)
• Hazel Panique (MSc)
• Zachary Teitel (PhD)