Differential gene expression reveals mechanisms related to habitat divergence between hybridizing orchids from the Neotropical coastal plains

Abstract

Background Closely related hybridizing species are ideal systems for identifying genomic regions underlying adaptive divergence. Although gene expression plays a central role in determining ecologically-based phenotypic differences, few studies have inferred the role of gene expression for adaptive divergence in Neotropical systems. In this study, we conduct genome-wide expression analysis alongside soil elemental analysis in sympatric and allopatric populations of Epidendrum fulgens and E. puniceoluteum (Orchidaceae), which occur in contrasting adjacent habitats in the Neotropical coastal plains. Results These species were highly differentiated by their gene expression profiles, as determined by 18–21% of transcripts. Gene ontology (GO) terms associated with reproductive processes were enriched according to comparisons between species in both allopatric and sympatric populations. Species showed differential expression in genes linked to salt and waterlogging tolerance according to comparisons between species in sympatry, and biological processes related to environmental stimulus appeared as representative among those transcripts associated with edaphic characteristics in each sympatric zone. Hybrids, in their turn, were well differentiated from E. fulgens, but exhibited a similar gene expression profile to flooding-tolerant E. puniceolutem. When compared with parental species, hybrids showed no transcripts with additive pattern of expression and increased expression for almost all transgressive transcripts. Conclusions This study sheds light on general mechanisms promoting ecological differentiation and assortative mating, and suggests candidate genes, such as those encoding catalase and calcium-dependent protein kinase, underling adaptation to harsh edaphic conditions in the Neotropical coastal plains. Moreover, it demonstrates that differential gene expression plays a central role in determining ecologically-based phenotypic differences among co-occurring species and their hybrids.

Hybridization: a ‘double-edged sword’ for Neotropical plant diversity

“…Given the ancient introgression in the ITS locus also observed in Central American Avicennia (Nettel et al, 2008), the authors suggested that interactions between hybridization and extrinsic factors (such as salinity and flooding tolerance) probably modulate diversification through passage of variants conferring adaptation to such extreme environments, as suggested in other species (e.g. Epidendrum: Pinheiro et al, 2010;Sujii et al, 2019;Leal et al, 2020).…”

“…Although there is also evidence of habitat-mediated selection shaping introgression across different habitats, the authors concluded that hybridization probably plays a significant evolutionary role and may increase the ecological amplitude of resultant offspring, as also shown in Marques et al (2014) and Sujii, Cozzolino & Pinheiro (2019). Recent transcriptomic work has also highlighted that hybrid individuals resulting from crossing of these two species preferentially express genes which code for flooding tolerance, as possessed by one of the parental species, and that hybridization underlies the generation of some of their phenotypic diversity (Leal et al, 2020), as suggested by morphological work on other Epidendrum spp. (Pansarin & Amaral, 2008).…”

“…This suggests that in terrestrial species hybrid offspring are more likely to persist for multiple generations and undergo backcrossing, eventually making detectable contributions to the genetic composition of parental species, as also shown in terrestrial Epidendrum spp. (Sujii et al, 2019;Leal et al, 2020) and Pitcairnia spp. (Wendt et al, 2001) on inselbergs.…”

Significance of introgression hybridization for extension of genetic variability in recipient genome

“…For example, [54] showed that introgression changes many phenotypic traits of Helianthus annuus that have an adaptive response to biotic and abiotic stresses. As was shown above, it is now clear that introgression causes the appearance of new traits not only due to the expected incorporation of alien chromatin into the host genome and its interaction with the resident genome, but also can generate new genetic and epigenetic variability in this genome [55][56][57][58][59].…”

Distribution of Biodiversity of Wild Beet Species (Genus Beta L.) in Armenia under Ongoing Climate Change Conditions

“…Natural hybridization is an important process in plant evolution that provides gene flow between genetically different populations or taxa, and may influence the adaptive response to selection, leading to the formation of a new species [ 61 ]. The role of gene expression for speciation is still relatively unexplored, despite the increasing number of studies characterizing candidate genes or describing general patterns of gene expression related to adaptive divergence in different systems [ 62 ].…”