Phenotypic variation and transgenerational responses of plants to different types of precipitation predictability
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2019
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Universidad Rey Juan Carlos
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BACKGROUND
Current climate change alters mean climatic conditions, weather variability, and environmental
predictability. Climatic models forecast strong increases in weather variability
and decreases of environmental predictability, i.e. in the level of temporal autocorrelation
of weather events. This suggests that in the future, organisms will face
great challenges. However, little experimental evidence for these predictions exists, and
the scarce experimental studies simulated droughts and/or extreme events, both being
detrimental for many organisms. Therefore, the effects of changes in environmental
predictability remain largely untested.
Environmental predictability is suggested to affect functional traits, phenotypic expression
and physiology, especially in sessile organisms like plants. More predictable
environments may pose fewer challenges, and theoretic studies suggest that they lead
to lower phenotypic variation. In contrast, less predictable environments are expected
to favour advances in phenology, potentially altering reproductive success, survival,
and population growth. Since plants derive important resources through their roots, root
investment strategies and their plasticity might be key to cope with changes in environmental
predictability. In addition, lower environmental predictability may entail greater
intra-population and intra-individual variability, and greater physiological changes,
which potentially affects ecosystem services. Finally, environmental predictability may
also affect the speed and direction of adaptive evolution, and the shape and strength of
selective regimes. Theoretic models further forecast that higher environmental predictability
favours adaptive evolution, while lower predictability rather leads to increased
phenotypic plasticity. However, these theoretical predictions remain largely untested.
OBJECTIVES
The general objective of this doctoral thesis is to experimentally test whether and how
lower precipitation predictability affects phenotypic and transgenerational responses of
two plant species: the common sainfoin Onobrychis viciifolia and the common poppy
Papaver rhoeas. The specific objectives are: First, investigating whether less predictable
precipitation leads to phenological changes, and whether they affect reproduction,
survival and population growth (Chapter 1 and 3). Second, testing whether and how less predictable precipitation affects the selective regime, root functional traits, root
investment strategies, and whether observed responses may affect plant performance
(Chapter 2). Third, testing whether environmental predictability mainly affects a given
life-stage or whether it affects all life-stages similarly (Chapter 1-5). Fourth, testing
whether the speed and direction of transgenerational responses depend on precipitation
predictability (Chapter 1-3). Fifth, testing whether rapid transgenerational responses
induced by differences in precipitation predictability are congruent with adaptive evolution
and/or with an increase in phenotypic plasticity (Chapter 1). Sixth, testing whether
less predictable precipitation modulates intra-population and intra-individual variation,
and reproduction, and whether observed changes are transmitted to the next generation
(Chapter 4). Seventh, investigating whether precipitation predictability changes physiological
response, and whether such changes may affect ecosystem services (Chapter 5).
METHODOLOGY
Seeds of Onobrychis viciifolia (Fabaceae) and Papaver rhoeas (Papaveraceae) were
sown during four consecutive years in experimental field plots situated at an experimental
research station located near Jaca (Huesca, Spain). More and less predictable
precipitation was simulated at daily and inter-seasonal time-scales, using an automatic
irrigation system. To test for treatment differences in phenology and reproduction, many
functional traits of both species were weekly measured. At the end of the annual cycle,
offspring seeds were individually collected, measured, and stored over the winter.
To test whether differences in precipitation predictability affected ecosystem services,
lignin, carbon and nitrogen content of the plant’s above- and below-ground parts were
determined. To test whether precipitation predictability affects the speed and direction
of transgenerational responses, three generations of stored offspring seeds (descendants)
were sown in the subsequent year. In each of the three years, descendants were
sown in the same plot, under the same precipitation conditions, and at the same time as
the ancestral seeds (i.e. seeds that were naive with regard to the simulated predictability
conditions), and their development trajectories and traits were compared. To disentangle
between evolutionary change and evolution of phenotypic plasticity, descendant
seeds of the second and third generation were planted in all treatment combinations.
RESULTS
Chapter 1 shows that lower short-term predictability of precipitation leads to phenological
advance and to an increase in reproductive success and population growth. Both
species exhibited rapid transgenerational responses that mitigated treatment differences observed in ancestors. The detected transgenerational responses were in line with increased
phenotypic plasticity, rather than a shift in trait expression. Moreover, transgenerational
responses mainly existed with respect to early growth conditions. Chapter 2
demonstrates that, in both species, root investment depends on precipitation predictability,
and that investment changes lead to increased performance. Moreover, precipitation
predictability induced differences in the strength of selection but not in the type of the
selective regime. Chapter 3 shows that decreased precipitation predictability enhances
seedling emergence, survival and reproductive rates in both species. Mainly treatment
during early growth affected survival and reproduction, while treatment during late
growth let to smaller differences. Descendants of P. rhoeas exhibited increased viability
compared to ancestors (in both treatments), and this difference was greater when
exposed to less predictable precipitation. Chapter 4 evidences that precipitation predictability
significantly affected intra-population and intra-individual variability, both
being greater when exposed to less predictable precipitation. Intra-individual variability
in reproductive traits is under stabilizing selection, and precipitation predictability
affected the location of the optima, optimal reproduction, as well as the strength of
selection, but not type of selection (i.e. stabilizing vs directional selection, etc). Chapter
5 demonstrates that less predictable precipitation led to lower lignin content, higher
ANPP (Aboveground Net Primary Productivity), more aboveground biomass, and higher
nitrogen content in roots and leaves. This shows that less predictable precipitation
altered plant physiology, which positively affected ecosystem services.
CONCLUSIONS
In contrast to the expected negative effects of decreased environmental predictability,
our study shows that at least some plant species may benefit from a lower precipitation
predictability, and that this positively affected ecosystem services. Earlier reproduction
observed in less predictable precipitation is in line with theory, but led to increased
reproductive success, survival, and population growth, rather than affecting them negatively.
This difference most likely exists, because the theoretical models assume that
earlier reproduction will be associated with shorter reproductive periods, while in this
study it was associated with a longer reproductive period. The positive responses are
also congruent with rapid and plastic responses exhibited by root functional traits, and
are in line with recent studies showing that plants were affected by the predictability of
soil nutrients. Less predictable precipitation increased intra-population variability but
also intra-individual variability, which demonstrates that intra individual variability is
a highly plastic trait that is under natural selection, rather than phenotypic noise. These results also suggests that higher intra-individual variance may affect population dynamics
and biodiversity. Moreover, under decreased precipitation predictability, plants
exhibited rapid transgenerational responses, which were congruent with increases in
phenotypic plasticity, and mainly existed with respect to precipitation predictability
during early growth. In contrast, reproduction of ancestors was chiefly affected by late
predictability. This suggests that it is important to consider the developmental stage at
which organisms are exposed to differences in environmental predictability, in evolutionary
and ecological theories. The findings reveal that many herbaceous plants may be
able to cope with increasing environmental uncertainties, thanks to investment changes,
existing, and evolving phenotypic plasticity. Therefore, to anticipate the impact of
climate change, theoretical models and mitigation efforts should take into account that
plants may rapidly respond to changes in climatic predictability, and that selective regimes
may change as well. This suggests that lower climatic predictability may induce
less biodiversity losses than expected by climatic models.
Descripción
Tesis Doctoral leída en la Universidad Rey Juan Carlos de Madrid en 2018. Director: Patrick S. Fitze
Tutor: José María Iriondo Alegría
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