skip to main content


Title: Convergent evolution of the annual life history syndrome from perennial ancestors

Despite most angiosperms being perennial, once-flowering annuals have evolved multiple times independently, making life history traits among the most labile trait syndromes in flowering plants. Much research has focused on discerning the adaptive forces driving the evolution of annual species, and in pinpointing traits that distinguish them from perennials. By contrast, little is known about how ‘annual traits’ evolve, and whether the same traits and genes have evolved in parallel to affect independent origins of the annual syndrome. Here, we review what is known about the distribution of annuals in both phylogenetic and environmental space and assess the evidence for parallel evolution of annuality through similar physiological, developmental, and/or genetic mechanisms. We then use temperate grasses as a case study for modeling the evolution of annuality and suggest future directions for understanding annual-perennial transitions in other groups of plants. Understanding how convergent life history traits evolve can help predict species responses to climate change and allows transfer of knowledge between model and agriculturally important species.

 
more » « less
Award ID(s):
2120732
NSF-PAR ID:
10472687
Author(s) / Creator(s):
; ; ; ;
Publisher / Repository:
Frontiers Media SA
Date Published:
Journal Name:
Frontiers in Plant Science
Volume:
13
ISSN:
1664-462X
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    We commonly use trait variation to characterize plant function within and among species and understand how vegetation responds to the environment. Seedling emergence is an especially vulnerable window affecting population and community dynamics, yet trait‐based frameworks often bypass this earliest stage of plant life. Here we assess whether traits vary in ecologically meaningful ways when seedlings are just days old. How do shared evolutionary history and environmental conditions shape trait expression, and can traits explain which seedlings endure drought?

    We measured seedling traits in the first 4 days of life for 16 annual plant species under two water treatments, exploring trait trade‐offs, species‐level plasticity and the ability of traits to predict duration of survival under drought.

    Nearly half of traits showed the imprint of evolutionary history (i.e. significant phylogenetic signal), often reflecting differences between grasses and forbs, two groups separated by a deep evolutionary split. Water availability altered trait expression in most cases, though species‐level plastic responses also reflected evolutionary history.

    On average, new seedlings exhibited substantial trait variation structured as multiple trade‐offs like those found in mature plants. Some species invested in thick roots and shoots, whereas others invested in more efficient tissues. Separately, some invested in tougher roots and others in deeper roots. We also observed trade‐offs related to growth rates (fast or slow) and biomass allocation (above‐ or below‐ground). Drought survival time was correlated most strongly with seed mass, root construction and allocation traits, and phylogeny (grasses vs. forbs).

    Synthesis.Our results show that seed and seedling trait variation among annual species is substantial, and that a few attributes could capture major dimensions of ecological strategies during emergence. With seedling survival times ranging twofold among annuals (from 7.5 to 14.5 days), these strategies could mitigate recruitment responses to more frequent or longer dry spells. Multivariate trait and plasticity strategies should be further explored in studies designed to assess trait‐fitness linkages during recruitment.

    A freePlain Language Summarycan be found within the Supporting Information of this article.

     
    more » « less
  2. Abstract

    Seasonal timing traits are commonly under recurrent, spatially variable selection, and are therefore predicted to exhibit clinal variation. Temperate perennial plants often require vernalization to prompt growth and reproduction; however, little is known about whether vernalization requirements change across the range of a broadly distributed species. We performed a critical vernalization duration study inMimulus ringens, coupled with population genomic analysis. Plants from eight populations spanning the latitudinal range were exposed to varying durations of 4°C vernalization between 0 and 56 days, and flowering response was assessed. RADSeq was also performed to generate 1179 polymorphic SNPs, which were used to examine population structure. We found unexpected life history variation, with some populations lacking vernalization requirement. Population genomic analyses show that these life history variants are highly divergent from perennials, potentially revealing a cryptic species. For perennial populations, minimum vernalization time was surprisingly consistent. However, once vernalized, northern populations flowered almost 3 weeks faster than southern. Furthermore, southern populations exhibited sensitivity to vernalization times beyond flowering competency, suggesting an ability to respond adaptively to different lengths of winter.Mimulus ringens, therefore, reveals evidence of clinal variation, and provides opportunities for future studies addressing mechanistic and ecological hypotheses both within and between incipient species.

     
    more » « less
  3. Abstract

    Local adaptation is common in plants, yet characterization of its underlying genetic basis is rare in herbaceous perennials. Moreover, while many plant species exhibit intraspecific chemical defence polymorphisms, their importance for local adaptation remains poorly understood. We examined the genetic architecture of local adaptation in a perennial, obligately‐outcrossing herbaceous legume, white clover (Trifolium repens). This widespread species displays a well‐studied chemical defence polymorphism for cyanogenesis (HCN release following tissue damage) and has evolved climate‐associated cyanogenesis clines throughout its range. Two biparental F2 mapping populations, derived from three parents collected in environments spanning the U.S. latitudinal species range (Duluth, MN, St. Louis, MO and Gainesville, FL), were grown in triplicate for two years in reciprocal common garden experiments in the parental environments (6,012 total plants). Vegetative growth and reproductive fitness traits displayed trade‐offs across reciprocal environments, indicating local adaptation. Genetic mapping of fitness traits revealed a genetic architecture characterized by allelic trade‐offs between environments, with 100% and 80% of fitness QTL in the two mapping populations showing significant QTL×E interactions, consistent with antagonistic pleiotropy. Across the genome there were three hotspots of QTL colocalization. Unexpectedly, we found little evidence that the cyanogenesis polymorphism contributes to local adaptation. Instead, divergent life history strategies in reciprocal environments were major fitness determinants: selection favoured early investment in flowering at the cost of multiyear survival in the southernmost site versus delayed flowering and multiyear persistence in the northern environments. Our findings demonstrate that multilocus genetic trade‐offs contribute to contrasting life history characteristics that allow for local adaptation in this outcrossing herbaceous perennial.

     
    more » « less
  4. BACKGROUND The Republic of Madagascar is home to a unique assemblage of taxa and a diverse set of ecosystems. These high levels of diversity have arisen over millions of years through complex processes of speciation and extinction. Understanding this extraordinary diversity is crucial for highlighting its global importance and guiding urgent conservation efforts. However, despite the detailed knowledge that exists on some taxonomic groups, there are large knowledge gaps that remain to be filled. ADVANCES Our comprehensive analysis of major taxonomic groups in Madagascar summarizes information on the origin and evolution of terrestrial and freshwater biota, current species richness and endemism, and the utilization of this biodiversity by humans. The depth and breadth of Madagascar’s biodiversity—the product of millions of years of evolution in relative isolation —is still being uncovered. We report a recent acceleration in the scientific description of species but many remain relatively unknown, particularly fungi and most invertebrates. DIGITIZATION Digitization efforts are already increasing the resolution of species richness patterns and we highlight the crucial role of field- and collections-based research for advancing biodiversity knowledge in Madagascar. Phylogenetic diversity patterns mirror that of species richness and endemism in most of the analyzed groups. Among the new data presented, our update on plant numbers estimates 11,516 described vascular plant species native to Madagascar, of which 82% are endemic, in addition to 1215 bryophyte species, of which 28% are endemic. Humid forests are highlighted as centers of diversity because of their role as refugia and centers of recent and rapid radiations, but the distinct endemism of other areas such as the grassland-woodland mosaic of the Central Highlands and the spiny forest of the southwest is also important despite lower species richness. Endemism in Malagasy fungi remains poorly known given the lack of data on the total diversity and global distribution of species. However, our analysis has shown that ~75% of the fungal species detected by environmental sequencing have not been reported as occurring outside of Madagascar. Among the 1314 species of native terrestrial and freshwater vertebrates, levels of endemism are extremely high (90% overall)—all native nonflying terrestrial mammals and native amphibians are found nowhere else on Earth; further, 56% of the island’s birds, 81% of freshwater fishes, 95% of mammals, and 98% of reptile species are endemic. Little is known about endemism in insects, but data from the few well-studied groups on the island suggest that it is similarly high. The uses of Malagasy species are many, with much potential for the uncovering of useful traits for food, medicine, and climate mitigation. OUTLOOK Considerable work remains to be done to fully characterize Madagascar’s biodiversity and evolutionary history. The multitudes of known and potential uses of Malagasy species reported here, in conjunction with the inherent value of this unique and biodiverse region, reinforce the importance of conserving this unique biota in the face of major threats such as habitat loss and overexploitation. The gathering and analysis of data on Madagascar’s remarkable biota must continue and accelerate if we are to safeguard this unique and highly threatened subset of Earth’s biodiversity. Emergence and composition of Madagascar’s extraordinary biodiversity. Madagascar’s biota is the result of over 160 million years of evolution, mostly in geographic isolation, combined with sporadic long distance immigration events and local extinctions. (Left) We show the age of the oldest endemic Malagasy clade for major groups (from bottom to top): arthropods, bony fishes, reptiles, flatworms, birds, amphibians, flowering plants, mammals, non-flowering vascular plants, and mollusks). Humans arrived recently, some 10,000 to 2000 years (top right) and have directly or indirectly caused multiple extinctions (including hippopotamus, elephant birds, giant tortoises, and giant lemurs) and introduced many new species (such as dogs, zebu, rats, African bushpigs, goats, sheep, rice). Endemism is extremely high and unevenly distributed across the island (the heat map depicts Malagasy palm diversity, a group characteristic of the diverse humid forest). Human use of biodiversity is widespread, including 1916 plant species with reported uses. The scientific description of Malagasy biodiversity has accelerated greatly in recent years (bottom right), yet the diversity and evolution of many groups remain practically unknown, and many discoveries await. 
    more » « less
  5. Abstract

    A critical tool in assessing ecosystem change is the analysis of long‐term data sets, yet such information is generally sparse and often unavailable for many habitats. Kelp forests are an example of rapidly changing ecosystems that are in most cases data poor. Because kelp forests are highly dynamic and have high intrinsic interannual variability, understanding how regional‐scale drivers are driving kelp populations—and particularly how kelp populations are responding to climate change—requires long‐term data sets. However, much of the work on kelp responses to climate change has focused on just a few, relatively long‐lived, perennial, canopy‐forming species. To understand how kelp populations with different life history traits are responding to climate‐related variability, we leverage 35 yr of Landsat satellite imagery to track the population size of an annual, ruderal kelp,Nereocystis luetkeana, across Oregon. We found high levels of interannual variability inNereocystiscanopy area and varying population trajectories over the last 35 yr. Surprisingly, OregonNereocystispopulation sizes were unresponsive to a 2014 marine heat wave accompanied by increases in urchin densities that decimated northern CaliforniaNereocystispopulations. Some OregonNereocystis populations have even increased in area relative to pre‐2014 levels. Analysis of environmental drivers found thatNereocystispopulation size was negatively correlated with estimated nitrate levels and positively correlated with winter wave height. This pattern is the inverse of the predicted relationship based on extensive prior work on the perennial kelpMacrocystis pyriferaand may be related to the annual life cycle ofNereocystis. This article demonstrates (1) the value of novel remote sensing tools to create long‐term data sets that may challenge our understanding of nearshore marine species and (2) the need to incorporate life history traits into our theory of how climate change will shape the ocean of the future.

     
    more » « less