Habitat preference of an herbivore shapes the habitat distribution of its host plant

Alexandre, Nicolas; Humphrey, Parris T.; Frazier, Joseph; Gloss, Andrew D.; Lee, Jimmy; Affeldt, H. A.; Whiteman, Noah K.

doi:10.1101/156240

Cited by 3 publications

(2 citation statements)

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“…It is critical, therefore, to sample multiple individuals when estimating species means, especially when assessing single plant species from a given locality (e.g. 8,9 ). Kozlov et al gathered too-few and too-variable specimens (n=1 to n=10 for ecological samples, and n=3 to n=20 for herbarium samples) to infer reliable estimates of herbivory.…”

Section: Main Textmentioning

confidence: 99%

Response to Kozlovet al.: Inaccurate estimation of biases in herbarium specimen data

Meineke¹,

Davis

Davies

2020

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SummaryKozlov and colleagues1 call into question the application of herbarium specimens to quantify historical patterns of herbivory2–5. It is already widely appreciated that collectors of herbarium specimens may tend to avoid insect damage, thus making herbivory estimates from herbarium specimens potentially down-biased2. However, Kozlov et al. additionally suggest that variation in sampling selectivity among collectors may misrepresent patterns of herbivory in nature. The authors sought to quantify these biases by collecting and contrasting insect herbivory data across 17 plant species from herbarium versus standard field ecological sampling procedures. They concluded that herbivory estimates from herbarium specimens are highly variable, rendering them an inaccurate representation of herbivory in nature. Our re-analysis of Kozlov et al.’s data, in contrast, reveals that herbarium specimens indeed provide a useful record of these symbioses. We demonstrate that Kozlov et al. were misled by analyzing comparisons derived from very few samples, which provide highly noisy estimates.

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Section: Main Textmentioning

confidence: 99%

Response to Kozlovet al.: Inaccurate estimation of biases in herbarium specimen data

Meineke¹,

Davis

Davies

2020

Preprint

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“…First, damage by the herbivore community of bittercress—and specifically by Scaptomyza nigrita (Drosophilidae), a specialist leaf-miner that can heavily defoliate stands of bittercress (Collinge and Louda 1989a; Gloss et al 2014)—is primarily restricted to sun habitats, and this has been consistently observed throughout many growing season across decades of study (Louda and Rodman 1983a,b; Louda 1984; Collinge and Louda 1989a,b; Louda and Rodman 1996; Alexandre et al 2018). Sun-biased herbivore pressure likely arises from a strong habitat preference of the herbivore (Alexandre et al 2018), which is thought to promote colonization of shade habitats by bittercress. As a consequence, the enemy free space associated with shade habitats would be expected to favor lower investment in anti-herbivore defenses (Agrawal et al 2012; Mooney et al 2016).…”

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confidence: 99%

Heritable plant phenotypes track light and herbivory levels at fine spatial scales

et al. 2018

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Organismal phenotypes often co-vary with environmental variables across broad geographic ranges. Less is known about the extent to which phenotypes match local conditions when multiple biotic and abiotic stressors vary at fine spatial scales. Bittercress (Brassicaceae: Cardamine cordifolia), a perennial forb, grows across a microgeographic mosaic of two contrasting herbivory regimes: high herbivory in meadows (sun habitats) and low herbivory in deeply shaded forest understories (shade habitats). We tested for local phenotypic differentiation in plant size, leaf morphology, and anti-herbivore defense (realized resistance and defensive chemicals, i.e., glucosinolates) across this habitat mosaic through reciprocal transplant-common garden experiments with clonally propagated rhizomes. We found habitat-specific divergence in morphological and defensive phenotypes that manifested as contrasting responses to growth in shade common gardens: weak petiole elongation and attenuated defenses in populations from shade habitats, and strong petiole elongation and elevated defenses in populations from sun habitats. These divergent phenotypes are generally consistent with reciprocal local adaptation: plants from shade habitats that naturally experience low herbivory show reduced investment in defense and an attenuated shade avoidance response, owing to its ineffectiveness within forest understories. By contrast, plants from sun habitats with high herbivory show shade-induced elongation, but no evidence of attenuated defenses canonically associated with elongation in shade-intolerant plant species. Finally, we observed differences in flowering phenology between habitat types that could potentially contribute to inter-habitat divergence by reducing gene flow. This study illuminates how clonally heritable plant phenotypes track a fine-grained mosaic of herbivore pressure and light availability in a native plant.

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Heritable plant phenotypes track light and herbivory levels at fine spatial scales

Humphrey

Gloss

Frazier

et al. 2017

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26The biotic and the abiotic environment play a major role in shaping plant 27 phenotypes and their geographic distributions. However, little is known about the 28 extent to which plant phenotypes match local patterns of herbivory across fine-29 grained habitat mosaics, despite the strong effect of herbivory on plant fitness. 30 Through a reciprocal transplant-common garden experiment with clonally 31 propagated rhizomes, we tested for local phenotypic differentiation in bittercress 32 (Brassicaceae: Cardamine cordifolia) plants collected across an ecotonal habitat 33 mosaic. We found that bittercress in sunny meadows (high herbivory) and shaded 34 understories (low herbivory) have diverged in heritable growth and herbivore 35 resistance phenotypes. The expression of these differences was habitat dependent, 36 mirroring patterns of adaptive divergence in phenotypic plasticity between plant 37 populations in meadow and understory habitats at broader geographic scales, and 38 showed no evidence for a constraint imposed by growth-defense tradeoffs. Most 39 notably, plants derived from shade habitats exhibited a weaker shade-induced 40 elongation response (i.e., shade avoidance syndrome, SAS) and reduced resistance 41 to herbivory, relative to plants derived from sun habitats, when both were grown in 42 shade common gardens. Greenhouse experiments revealed that divergent SAS 43 phenotypes in shade conditions were expressed in offspring grown from seed as well. 44Finally, we observed partially non-overlapping flowering phenology between 45 habitat-types in the field, which may be at least one factor that helps to reinforce 46 habitat-specific phenotypic divergence. Altogether, our study illuminates how a 47 48 grained habitat mosaic. 49 50 51 55 2005; Richardson et al. 2014). However, our knowledge regarding the conditions 56 under which these patterns arise and persist has been disproportionately shaped by 57 studies at course-grained rather than fine-grained spatial scales (Richardson et al.58 2014). This bias has likely been shaped by the expectation that gene flow among 59 interspersed habitat patches is generally a strong homogenizing force, preventing 60 the establishment of habitat-associated phenotypic and genotypic variation at fine-61 grained spatial scales (Haldane 1930; Lenormand 2002). Although there is growing 62 evidence that heritable phenotypes track habitat mosaics at fine-grained spatial 63 3 scales [i.e. microgeographic phenotypic divergence; (Richardson et al. 2014)] we 64 have a limited understanding of the molecular, ecological, and evolutionary 65 processes that facilitate and maintain this variation in nature. 66 67 Defoliation by insect herbivores exerts strong selection on plant phenotypes (Louda 68 1984; Prasad et al. 2012; Agrawal et al. 2012). In mustards (Brassicaceae), 69 polymorphisms in genes that modify defensive chemicals underlie adaptation to 70 local herbivore communities (Prasad et al. 2012; Zust et al. 2012), and the 71 magnitude of geographic divergence at such loci is extr...

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Habitat preference of an herbivore shapes the habitat distribution of its host plant

Cited by 3 publications

References 29 publications

Response to Kozlovet al.: Inaccurate estimation of biases in herbarium specimen data

Response to Kozlovet al.: Inaccurate estimation of biases in herbarium specimen data

Heritable plant phenotypes track light and herbivory levels at fine spatial scales

Heritable plant phenotypes track light and herbivory levels at fine spatial scales

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