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Plant-insect interactions and the evolution of polyploidy in Lithophragma bolanderi

Romero-Bravo, Andrés (2020) BION02 20192
Degree Projects in Biology
Abstract
Plant-insect interactions play a crucial role in the evolution of the coevolving web of life, shaping local interaction networks and moulding the diversity and the evolutionary history of two of the most diverse groups of organisms on earth. The interaction between Lithophragma bolanderi (Saxifragaceae), which presents a geographic mosaic of ploidy levels, and the pollinating floral parasite Greya politella (Prodoxidae) poses an interesting study system to assess how these local interaction networks evolve. Polyploidization events, one of the major drivers of speciation in plant evolution, are known to have occurred in L. bolanderi and, together with changes in reproductive strategies, can determine how plants allocate resources to sexual... (More)
Plant-insect interactions play a crucial role in the evolution of the coevolving web of life, shaping local interaction networks and moulding the diversity and the evolutionary history of two of the most diverse groups of organisms on earth. The interaction between Lithophragma bolanderi (Saxifragaceae), which presents a geographic mosaic of ploidy levels, and the pollinating floral parasite Greya politella (Prodoxidae) poses an interesting study system to assess how these local interaction networks evolve. Polyploidization events, one of the major drivers of speciation in plant evolution, are known to have occurred in L. bolanderi and, together with changes in reproductive strategies, can determine how plants allocate resources to sexual and asexual reproduction through metabolic changes. However, the interactions between polyploidization and nursery pollination systems like the one involving Lithophragma and Greya, remain unclear. In this study, I adopt a combined approach including molecular analyses to elucidate the origin of polyploid populations of L. bolanderi, and a series of experimental analyses using data collected in the field and in commongarden experiments to determine how investment in sexual and asexual reproductive traits can affect, and be affected by, the interaction between L. bolanderi and G. politella. I found that an allopolyploidization event with the congener L. glabrum gave rise to a tetraploid L. bolanderi lineage. The hexaploid individuals also have alleles diagnostic of L. glabrum, and could hence have arisen, for example, through spontaneous chromosome doubling in an unstable triploid formed after a diploid-tetraploid hybridization. A sprouting experiment indicated that a higher investment in asexual reproduction correlates with higher sprouting rates. A hand-pollination experiment showed a strong resource-allocation trade-off between sexual and asexual reproduction. A common-garden setup showed that the investment of diploid L. bolanderi populations in asexual reproduction presents a large variation determined by local genotypes. However, data collection from natural populations showed a positive correlation between sexual reproductive fitness and asexual reproduction in diploid populations. Surprisingly, predictors of asexual reproductive fitness correlated positively with altitude while predictors of sexual reproductive fitness presented a negative correlation with G. politella visitation rates in diploid populations, but not in polyploids. Additionally, the interaction with G. politella showed negative effects on sexual reproductive fitness in diploid populations, but not in polyploid populations of L. bolanderi. This study highlights that both plant-pollinator interactions and polyploidization relate to each other through changes in pollination systems and reproductive strategies, contributing to the evolution of local plant-insect interaction networks. (Less)
Popular Abstract
Unveiling the story of pollination and plants with multiple genomes

In an era characterised by unprecedented anthropogenic climate change and mass extinction, it is extremely important to understand the processes generating and maintaining biodiversity and ecosystems. Among these processes, pollination is a crucial mechanism that shapes ecological networks. It involves different groups of organisms in complex and long-lasting interactions that have been occurring for several hundreds of millions of years, driving the evolution of plants and insects. Nowadays, pollinators are experiencing a general decline all around the world. One way for plants to assure reproduction when pollinators are scarce is clonal reproduction. Producing clones... (More)
Unveiling the story of pollination and plants with multiple genomes

In an era characterised by unprecedented anthropogenic climate change and mass extinction, it is extremely important to understand the processes generating and maintaining biodiversity and ecosystems. Among these processes, pollination is a crucial mechanism that shapes ecological networks. It involves different groups of organisms in complex and long-lasting interactions that have been occurring for several hundreds of millions of years, driving the evolution of plants and insects. Nowadays, pollinators are experiencing a general decline all around the world. One way for plants to assure reproduction when pollinators are scarce is clonal reproduction. Producing clones can also help plants to reproduce when other factors hinder sexual reproduction. When plants duplicate their entire genome, they cannot correctly reproduce through pollination with the rest of “normal” individuals of their species. The event in which a plant duplicates all its genome is called polyploidization. Polyploidization can have profound effects on genes and since genes control, among others, floral characters involved in attracting pollinators (such as scent, shape or size of the flowers) polyploidization could affect plant-pollinator interactions.

This study aims to describe how polyploidization can occur and how it affects, and is affected by, plant-insect interactions and reproductive strategies in plants. The Bolander's woodland star (Lithophragma bolanderi) is an excellent plant species to address the aims of this study since it has an interesting pollination system. An important pollinator of this plant is the diurnal moth called Greya politella. This moth transfers pollen between the flowers while laying eggs into them. The larvae of this moth feed on part of the seeds of the plant. At the same time, since the moth only visits plants of the same genus, the plant gets a highly efficient pollination service in exchange for some seed loss. Thus, this interaction is considered to be mutualistic, since organisms in both parts benefit from each other. But this woodland star can also produce clones through special root structures called bulbils. Thus, it can reproduce without the help of any pollinator.
In addition, in some locations, L. bolanderi has multiple genomes instead of only one. This study found that all plants of the Bolander's woodland star with multiple genomes might have resulted from one or several past hybridisation events with the bulbous woodland star (Lithophragma glabrum).

Resources, pollinators and environment
Since flowers and seeds are expensive to produce and since the resources of a plant are limited, the lower the seed set the more resources available for producing bulbils and the more easily the plants will produce new clones. Thus, no need for pollinators means no seeds eaten by the larvae and therefore less "waste" of resources. Through experiments in the greenhouse and in the lab, this study found that the woodland star splits the available resources between seed and bulbil production in a balanced fashion and that the larger its bulbils are, the more easily the woodland stars produce new clones. Therefore, since the amount of resources a plant spends on producing bulbils is determined by its genes, polyploidization could have effects on its reproduction.
In relation to its relationship with Greya moths, this study also found that plants with multiple genomes suffer less negative effects when being pollinated by the moth than the plants with only one genome. This could affect how many resources these plants "waste" in seeds eaten by the larvae of the moths and therefore how many resources they can spend in producing new clonal plants. However, this and other recent studies found that moths are not the only pollinators. Other insects, such as bees and flies, also visit Bolander’s woodland star without eating any of its seeds. This study also indicates that environmental agents other than pollinators might also affect resource management in this species: altitude or temperature might also affect the interaction between Bolander’s woodland star and its specialized moth pollinator.

Understanding diversity to be able to conserve it
The current pollinator decline all around the globe could significantly affect plant diversity in a very dramatic way. Learning more about the relationship between plant-pollinator interactions and the relative investment in different reproduction strategies in plants with multiple genomes could help us to understand and predict how environmental changes might affect pollination. It will also teach us which factors are more important to consider when it comes to the conservation of the ecosystem functions that maintain the biodiversity on which every species, including humans, rely.

Master’s Degree Project in Biology, 45 credits, 2020.
Department of Biology, Lund University

Advisors: Magne Friberg, Anna Runemark and Karin Gross
Evolutionary Ecology of Plant-Insect Interactions Group (Less)
Please use this url to cite or link to this publication:
author
Romero-Bravo, Andrés
supervisor
organization
course
BION02 20192
year
type
H2 - Master's Degree (Two Years)
subject
language
English
id
9028990
date added to LUP
2020-09-14 10:49:48
date last changed
2020-09-14 10:49:48
@misc{9028990,
  abstract     = {Plant-insect interactions play a crucial role in the evolution of the coevolving web of life, shaping local interaction networks and moulding the diversity and the evolutionary history of two of the most diverse groups of organisms on earth. The interaction between Lithophragma bolanderi (Saxifragaceae), which presents a geographic mosaic of ploidy levels, and the pollinating floral parasite Greya politella (Prodoxidae) poses an interesting study system to assess how these local interaction networks evolve. Polyploidization events, one of the major drivers of speciation in plant evolution, are known to have occurred in L. bolanderi and, together with changes in reproductive strategies, can determine how plants allocate resources to sexual and asexual reproduction through metabolic changes. However, the interactions between polyploidization and nursery pollination systems like the one involving Lithophragma and Greya, remain unclear. In this study, I adopt a combined approach including molecular analyses to elucidate the origin of polyploid populations of L. bolanderi, and a series of experimental analyses using data collected in the field and in commongarden experiments to determine how investment in sexual and asexual reproductive traits can affect, and be affected by, the interaction between L. bolanderi and G. politella. I found that an allopolyploidization event with the congener L. glabrum gave rise to a tetraploid L. bolanderi lineage. The hexaploid individuals also have alleles diagnostic of L. glabrum, and could hence have arisen, for example, through spontaneous chromosome doubling in an unstable triploid formed after a diploid-tetraploid hybridization. A sprouting experiment indicated that a higher investment in asexual reproduction correlates with higher sprouting rates. A hand-pollination experiment showed a strong resource-allocation trade-off between sexual and asexual reproduction. A common-garden setup showed that the investment of diploid L. bolanderi populations in asexual reproduction presents a large variation determined by local genotypes. However, data collection from natural populations showed a positive correlation between sexual reproductive fitness and asexual reproduction in diploid populations. Surprisingly, predictors of asexual reproductive fitness correlated positively with altitude while predictors of sexual reproductive fitness presented a negative correlation with G. politella visitation rates in diploid populations, but not in polyploids. Additionally, the interaction with G. politella showed negative effects on sexual reproductive fitness in diploid populations, but not in polyploid populations of L. bolanderi. This study highlights that both plant-pollinator interactions and polyploidization relate to each other through changes in pollination systems and reproductive strategies, contributing to the evolution of local plant-insect interaction networks.},
  author       = {Romero-Bravo, Andrés},
  language     = {eng},
  note         = {Student Paper},
  title        = {Plant-insect interactions and the evolution of polyploidy in Lithophragma bolanderi},
  year         = {2020},
}