Hybridization Slows Rate of Evolution in Crop-Wild Compared to Wild Populations of Weedy Raphanus Across a Moisture Gradient

Abstract

Hybrid offspring of crops and their wild relatives commonly possess non-adaptive phenotypes and diminished fitness. Regularly, diminished success in early-generation hybrid populations is interpreted to suggest reduced biosafety risk regarding the unintended escape of novel traits from crop populations. Yet hybrid populations have been known to evolve to recover fitness relative to wild progenitors and can do so more rapidly than wild populations, although rates of evolution (for both hybrid populations and their wild progenitors) are sensitive to environmental context. In this research, we asked whether hybrid populations evolved more rapidly than wild populations in the context of soil moisture. We estimated evolutionary rates for 40 Raphanus populations that varied in their history of hybridization and environmental context (imposed by an experimental moisture cline) in two common gardens. After five generations of growing wild and crop-wild hybrid populations across a soil-moisture gradient, hybrid populations exhibited increased seedling emergence frequencies (~6% more), earlier emergence (~1 day), later flowering (~3 days), and larger body size (15–35%)—traits correlated with fitness—relative to wild populations. Hybrid populations, however, exhibited slower evolutionary rates than wild populations. Moreover, the rate of evolution in hybrid populations was consistent across evolutionary watering environments, but varied across watering environments in wild populations. These consistent evolutionary rates exhibited in hybrid populations suggests the evolution of robust traits that perform equally across soil moisture environments—a survival strategy characterized as “jack of all trades.” Although, diverse integrated weed management practices must be applied to wild and hybrid genotypes to diversify selection on these populations, evaluating the evolutionary rates of weeds in diverse environments will support the development of multi-faceted weed control strategies and effective integrated weed management policies.

The role of intraspecific crop-weed hybridization in the evolution of weediness and invasiveness: cultivated and weedy radish (Raphanus sativusL.) as a case study

“…Contrary to our expectation, our results showed higher plant biomass and fecundity and consequently higher relative fitness in the reciprocal crop-weed hybrids compared to their parents in both contrasting environments, indicating that the result of the crop-weed hybridization was environmental independent. Also, no biotype by environment interaction was found in crop-weed radish hybrids from North America in response to diverse watering environments (Shukla et al, 2020). Because ecological conditions rarely, if ever, reversed the relative performance of hybrids compared with their parents (Campbell and Snow 2007, and references therein), our results suggest that reciprocal crop-weed hybridization has the .…”

“…Contrary to our expectation, our results showed higher plant biomass and fecundity and consequently higher relative fitness in the reciprocal crop-weed hybrids compared to their parents in both contrasting environments, indicating that the result of the crop-weed hybridization was environmental independent. Also, no biotype by environment interaction was found in crop-weed radish hybrids from North America in response to diverse watering environments (Shukla et al, 2020). Because ecological conditions rarely, if ever, reversed the relative performance of hybrids compared with their parents (Campbell and Snow 2007, and references therein), our results suggest that reciprocal crop-weed hybridization has the potential to increase weediness and invasiveness in a wide range of environmental conditions (e.g., both inside and outside the agricultural environment), and could increase the chances of success when hybrids invade new environments or are exposed to environmental changes as a result of ongoing climate change (Hovick et al, 2012; Clements and Jones, 2021).…”

“…These studies allow the acceleration of natural processes in order to explore local ecological scenarios under which the fitness of crop-weed hybrids may equal or exceed the fitness of their parents, favoring the persistence of crop alleles in wild/weedy populations and consequently enhancing weediness and invasiveness (Mercer et al, 2006;Campbell et al, 2009). The Raphanus complex, formed by the cultivated species R. sativus, their feral conspecific forms and their weedy related species R. raphanistrum, is a well-established model system that has been widely used to evaluate the ecological and evolutionary consequences of interspecific crop-weed hybridization (Campbell et al, 2006(Campbell et al, , 2009Hegde et al, 2006;Campbell and Snow, 2007;Ridley et al, 2008;Snow et al, 2010;Hovick et al, 2012;Shukla et al, 2020Shukla et al, , 2021. Evolutionary experiments are often necessary for the observation and characterization of evolutionary changes occurring as a consequence of natural crop-wild/weed hybridization processes (Ellstrand et al, 2010;Hovick and Whitney, 2014).…”

No Correlation Between Pollen Fertility and Viability: Differential Measures of Male Gametophytic Fitness inCannabis sativaL.

“…While there is a substantial body of literature estimating the relative fitness of pollen (Choi et al, 2014;Hauser and Siegismund, 2000;Hudson and Stewart, 2004;Luria et al, 2019;McDowell et al, 2015), the terminology used to describe these characteristics is inconsistent. Though some authors correctly differentiate between fertility and viability (Barrow, 1983;Dafni and Firmage, 2000;Rajasekharan and Ganeshan, 1994;Trognitz, 1991), others use the terms interchangeably as synonyms, reflecting broad misconceptions of these terms (Qureshi et al, 2009;Shukla et al, 2020;Tuinstra and Wedel, 2000). Definitively, viability measures cytoplasmic degradation of the regenerative cell to quantify the proportion of pollen from a sire containing intact regenerative nuclei (Alexander, 1969;Atlagić et al, 2012;Barrow, 1983;De Souza et al, 2003;Firmage and Dafni, 2000;Heslop-Harrison and Heslop-Harrison, 1970;Impe et al, 2020;Khatun and Flowers, 1995;Pinillos and Cuevas, 2008;Rao et al, 1992;Rich, 2009;Rodriguez-Riano and Dafni, 2000;Shivanna and Heslop-Harrison, 1981).…”

The role of intraspecific crop–weed hybridization in the evolution of weediness and invasiveness: Cultivated and weedy radish (Raphanus sativus) as a case study

“…These studies allow the acceleration of natural processes to evaluate local ecological scenarios in which the fitness of crop-weed hybrids may equal or exceed the fitness of their parents, favoring the persistence of crop alleles in wild/weedy populations and consequently enhancing weediness and invasiveness (Mercer et al, 2006;Campbell et al, 2009). The Raphanus complex, formed by the cultivated species R. sativus, their weedy conspecific forms, and their related weed species, R. raphanistrum, is a well-established model system for evaluating the ecological and evolutionary consequences of interspecific crop-weed hybridization (Campbell et al, 2006(Campbell et al, , 2009Hegde et al, 2006;Campbell and Snow, 2007;Ridley et al, 2008;Snow et al, 2010;Hovick et al, 2012;Shukla et al, 2020Shukla et al, , 2021. We compared the time to flowering, survival to maturity, plant biomass, and reproductive components of bidirectional firstgeneration crop-weed hybrids in relation to both parents under two contrasting ecological environments, agrestal (wheat cultivation, fertilization, weeding) and ruderal (human-disturbed uncultivated area) over 2 years.…”