Coexistence of Trichome Variation in a Natural Plant Population: A Combined Study Using Ecological and Candidate Gene Approaches

Abstract

The coexistence of distinct phenotypes within populations has long been investigated in evolutionary ecology. Recent studies have identified the genetic basis of distinct phenotypes, but it is poorly understood how the variation in candidate loci is maintained in natural environments. In this study, we examined fitness consequences and genetic basis of variation in trichome production in a natural population of Arabidopsis halleri subsp. gemmifera. Half of the individuals in the study population produced trichomes while the other half were glabrous, and the leaf beetle Phaedon brassicae imposed intensive damage to both phenotypes. The fitness of hairy and glabrous plants showed no significant differences in the field during two years. A similar result was obtained when sibling hairy and glabrous plants were transplanted at the same field site, whereas a fitness cost of trichome production was detected under a weak herbivory condition. Thus, equivalent fitness of hairy and glabrous plants under natural herbivory allows their coexistence in the contemporary population. The pattern of polymorphism of the candidate trichome gene GLABROUS1 (GL1) showed no evidence of long-term maintenance of trichome variation within the population. Although balancing selection under fluctuating biotic environments is often proposed to explain the maintenance of defense variation, the lack of clear evidence of balancing selection in the study population suggests that other factors such as gene flow and neutral process may have played relatively large roles in shaping trichome variation at least for the single population level.

Associational effects against a leaf beetle mediate a minority advantage in defense and growth between hairy and glabrous plants

“…After flowering, plants develop leaves and roots on the primary and axillary meristems of the flowering stems, and these new rosettes establish as clonal offspring by rooting into the ground. The presence/absence of trichomes is associated with the allelic status of a trichome-related gene, GL1, but not with its flanking regions or other genes (Kawagoe et al 2011). Hairy plants develop nonglandular trichomes on the surfaces of leaves and stems, whereas glabrous plants have no trichomes except for on the leaf margins.…”

“…Trichomes also function in the tolerance to abiotic stresses (Wagner et al 2004). Moreover, trichomes impose a cost on plant growth and/or reproduction (Sletvold et al 2010;Kawagoe et al 2011;Züst et al 2011). To test intraspecific associational effects and their frequency dependence, we focused on trichome production as a representative trait of plant defense that exhibited genetic polymorphism.…”

“…gemmifera (Matsum.) O'Kane & Al-Shehbaz [Brassicaceae/Cruciferae: referred to as A. halleri, hereafter] possesses a genetic dimorphism of trichome-producing (hairy) and trichomeless (glabrous) morphs (Kawagoe et al 2011). For this subspecies, Kawagoe et al (2011) determined the reproductive cost for the production of trichomes.…”

“…O'Kane & Al-Shehbaz [Brassicaceae/Cruciferae: referred to as A. halleri, hereafter] possesses a genetic dimorphism of trichome-producing (hairy) and trichomeless (glabrous) morphs (Kawagoe et al 2011). For this subspecies, Kawagoe et al (2011) determined the reproductive cost for the production of trichomes. In an evaluation of the anti-herbivore resistance conferred by trichomes, Sato et al (2014) reports that an oligophagous beetle Phaedon brassicae Baly [Coleoptera: Chrysomelidae] preferred to feed on glabrous leaves and avoided hairy leaves only when the latter leaf type was rare.…”

Natural Variation in Arabidopsis: From Molecular Genetics to Ecological Genomics

“…Balancing selection, however, which is often taken as a sign of trade-offs, does not appear to be responsible for maintaining different GL1 alleles (Hauser et al, 2001). Glabrousness caused by inactivating mutations in GL1 also segregates in A. lyrata and Arabidopsis halleri populations (Hauser et al, 2001;Kärkkäinen and Å gren, 2002;Kivimäki et al, 2007;Kawagoe et al, 2011).…”