scholarly journals C4 photosynthesis and climate through the lens of optimality

2018 ◽  
Vol 115 (47) ◽  
pp. 12057-12062 ◽  
Author(s):  
Haoran Zhou ◽  
Brent R. Helliker ◽  
Matthew Huber ◽  
Ashley Dicks ◽  
Erol Akçay

CO2, temperature, water availability, and light intensity were all potential selective pressures that determined the competitive advantage and expansion of the C4 photosynthetic carbon-concentrating mechanism over the last ∼30 My. To tease apart how selective pressures varied along the ecological trajectory of C4 expansion and dominance, we coupled hydraulics to photosynthesis models while optimizing photosynthesis over stomatal resistance and leaf/fine-root allocation. We further examined the importance of nitrogen reallocation from the dark to the light reactions. We show here that the primary selective pressures favoring C4 dominance changed through the course of C4 evolution. The higher stomatal resistance and leaf-to-root ratios enabled by C4 led to an advantage without any initial difference in hydraulic properties. We further predict a reorganization of the hydraulic system leading to higher turgor-loss points and possibly lower hydraulic conductance. Selection on nitrogen reallocation varied with CO2 concentration. Through paleoclimate model simulations, we find that water limitation was the primary driver for a C4 advantage, with atmospheric CO2 as high as 600 ppm, thus confirming molecular-based estimates for C4 evolution in the Oligocene. Under these high-CO2 conditions, nitrogen reallocation was necessary. Low CO2 and high light, but not nitrogen reallocation, were the primary drivers for the mid- to late-Miocene global expansion of C4. We also predicted the timing and spatial distribution for origins of C4 ecological dominance. The predicted origins are broadly consistent with prior estimates, but expand upon them to include a center of origin in northwest Africa and a Miocene-long origin in Australia.

2016 ◽  
Author(s):  
Haoran Zhou ◽  
Brent R. Helliker ◽  
Erol Akçay

AbstractCO2, temperature, water availability and light intensity were all potential selective pressures to propel the initial evolution and global expansion of C4 photosynthesis over the last 30 million years. To tease apart how the primary selective pressures varied along this evolutionary trajectory, we coupled photosynthesis and hydraulics models while optimizing photosynthesis over stomatal resistance and leaf/fine-root allocation. We further examined the importance of resource (e.g. nitrogen) reallocation from the dark to the light reactions during and after the initial formation of C4 syndrome. We show here that the primary selective pressures—all acting upon photorespiration in C3 progenitors—changed through the course of C4 evolution. The higher stomatal resistance and leaf-to-root allocation ratio enabled by the C4 carbon-concentrating mechanism led to a C4 advantage without any change in hydraulic properties, but selection on nitrogen reallocation varied. Water limitation was the primary driver for the initial evolution of C4 25-32 million years ago, and could positively select for C4 evolution with atmospheric CO2 as high as 600 ppm. Under these high CO2 conditions, nitrogen reallocation was necessary. Low CO2 and light intensity, but not nitrogen reallocation, were the primary drivers during the global radiation of C4 5-10 MYA. Finally, our results suggest that identifying the predominate selective pressures at the time C4 first evolved within a lineage should help explain current biogeographical distributions.Statement of authorship:HZ, BH and EA conceptualized the study. HZ and EA built the model, HZ and BH put the idea in a general evolutionary context, HZ performed the modeling work and analyzed output data. HZ wrote the first draft, BH and EA contributed substantially to revisions.Significance StatementC4 photosynthesis pathway had evolved more than 60 times independently across the terrestrial plants through mid-Oligocene (~30 MYA) and diversified at late Miocene (5 to 10 MYA). We use an optimal physiology model to examine the primary selective pressures along the evolutionary history. Water limitation was the primary driver for C4 evolution from the initial evolutionary events 25-32 MYA until CO2 became low enough to, along with light intensity, drive the global radiation of C4 5-10 MYA. This modeling framework can be used to investigate evolution of other physiological traits (e.g. N reallocation, hydraulics) after the initial formation of C4 syndrome, which contributed to further increasing productivity of C4 in historical and current environmental conditions.


Author(s):  
Christian Peeters ◽  
Roberto A. Keller ◽  
Adam Khalife ◽  
Georg Fischer ◽  
Julian Katzke ◽  
...  

Abstract Background Explanations for the ecological dominance of ants generally focus on the benefits of division of labour and cooperation during foraging. However, the principal innovation of ants relative to their wasp ancestors was the evolution of a new phenotype: a wingless worker caste optimized for ground labour. Ant workers are famous for their ability to lift and carry heavy loads, but we know surprisingly little about the morphological basis of their strength. Here we examine the consequences of the universal loss of flight in ant workers on skeletomuscular adaptations in the thorax for enhanced foraging on six legs. Results Using X-ray microcomputed tomography and 3D segmentation, we compared winged queens and wingless workers in Euponera sikorae (subfamily Ponerinae) and Cataglyphis savignyi (subfamily Formicinae). Workers are characterized by five major changes to their thorax: i) fusion of the articulated flight thorax (queens) into a rigid box optimized to support the muscles that operate the head, legs and abdomen, ii) redesign of internal cuticular structures for better bracing and muscle attachment, iii) substantial enlargement of the neck muscles for suspending and moving the head, iv) lengthening of the external trochanter muscles, predominant for the leg actions that lift the body off the ground, v) modified angle of the petiole muscles that are key for flexion of the abdomen. We measured volumes and pennation angles for a few key muscles to assess their increased efficacy. Our comparisons of additional workers across five genera in subfamilies Dorylinae and Myrmicinae show these modifications in the wingless thorax to be consistent. In contrast, a mutillid wasp showed a different pattern of muscle adaptations as a result of the lack of wing muscles. Conclusions Rather than simply a subtraction of costly flight muscles, we propose the ant worker thorax evolved into a power core underlying stronger mandibles, legs, and sting. This contrasts with solitary flightless insects where the lack of central place foraging generated distinct selective pressures for rearranging the thorax. Stronger emphasis is needed on innovations of social insects as individuals at the phenotypic level to further our understanding of the evolution of social behaviours.


2020 ◽  
Vol 17 (1) ◽  
Author(s):  
Christian Peeters ◽  
Roberto A. Keller ◽  
Adam Khalife ◽  
Georg Fischer ◽  
Julian Katzke ◽  
...  

Abstract Background Explanations for the ecological dominance of ants generally focus on the benefits of division of labour and cooperation during foraging. However, the principal innovation of ants relative to their wasp ancestors was the evolution of a new phenotype: a wingless worker caste optimized for ground labour. Ant workers are famous for their ability to lift and carry heavy loads, but we know surprisingly little about the morphological basis of their strength. Here we examine the consequences of the universal loss of flight in ant workers on skeletomuscular adaptations in the thorax for enhanced foraging on six legs. Results Using X-ray microcomputed tomography and 3D segmentation, we compared winged queens and wingless workers in Euponera sikorae (subfamily Ponerinae) and Cataglyphis savignyi (subfamily Formicinae). Workers are characterized by five major changes to their thorax: i) fusion of the articulated flight thorax (queens) into a rigid box optimized to support the muscles that operate the head, legs and abdomen, ii) redesign of internal cuticular structures for better bracing and muscle attachment, iii) substantial enlargement of the neck muscles for suspending and moving the head, iv) lengthening of the external trochanter muscles, predominant for the leg actions that lift the body off the ground, v) modified angle of the petiole muscles that are key for flexion of the abdomen. We measured volumes and pennation angles for a few key muscles to assess their increased efficacy. Our comparisons of additional workers across five genera in subfamilies Dorylinae and Myrmicinae show these modifications in the wingless thorax to be consistent. In contrast, a mutillid wasp showed a different pattern of muscle adaptations resulting from the lack of wing muscles. Conclusions Rather than simply a subtraction of costly flight muscles, we propose the ant worker thorax evolved into a power core underlying stronger mandibles, legs, and sting. This contrasts with solitary flightless insects where the lack of central place foraging generated distinct selective pressures for rearranging the thorax. Stronger emphasis is needed on morphological innovations of social insects to further our understanding of the evolution of social behaviours.


2020 ◽  
Author(s):  
Christian Peeters ◽  
Roberto A. Keller ◽  
Adam Khalife ◽  
Georg Fischer ◽  
Julian Katzke ◽  
...  

Abstract Background Explanations for the ecological dominance of ants generally focus on the benefits of division of labour and cooperation during foraging. However, the principal innovation of ants relative to their wasp ancestors was the evolution of a new phenotype: a wingless worker caste optimized for ground labour. Ant workers are famous for their ability to lift and carry heavy loads, but we know surprisingly little about the morphological basis of their strength. Here we examine the consequences of the universal loss of flight in ant workers on skeletomuscular adaptations in the thorax for enhanced foraging on six legs. Results Using X-ray microcomputed tomography and 3D segmentation, we compared winged queens and wingless workers in Euponera sikorae (subfamily Ponerinae) and Cataglyphis savignyi (subfamily Formicinae). Workers are characterized by five major changes to their thorax: i) fusion of the articulated flight thorax (queens) into a rigid box optimized to support the muscles that operate the head, legs and abdomen, ii) redesign of internal cuticular structures for better bracing and muscle attachment, iii) substantial enlargement of the neck muscles for suspending and moving the head, iv) lengthening of the external trochanter muscles, predominant for the leg actions that lift the body off the ground, v) modified angle of the petiole muscles that are key for flexion of the abdomen. We measured volumes and pennation angles for a few key muscles to assess their increased efficacy. Our comparisons of additional workers across five genera in subfamilies Dorylinae and Myrmicinae show these modifications in the wingless thorax to be consistent. In contrast, a mutillid wasp showed a different pattern of muscle adaptations as a result of the lack of wing muscles. Conclusions Rather than simply a subtraction of costly flight muscles, we propose the ant worker thorax evolved into a power core underlying stronger mandibles, legs, and sting. This contrasts with solitary flightless insects where the lack of central place foraging generated distinct selective pressures for rearranging the thorax. Stronger emphasis is needed on innovations of social insects as individuals at the phenotypic level to further our understanding of the evolution of social behaviours.


Trees ◽  
2021 ◽  
Author(s):  
Jorma Zimmermann ◽  
Roman M. Link ◽  
Markus Hauck ◽  
Christoph Leuschner ◽  
Bernhard Schuldt

Abstract Key message By combining dendrochronological time-series analysis with radial vessel features, we show that the reconstruction of hydraulic properties improves our understanding of tree species’ acclimation potential to climate change. Abstract The vascular architecture plays a crucial role in the productivity and drought tolerance of broadleaf trees, but it is not yet fully understood how the hydraulic system is acclimating to a warmer and drier climate. Because vessel features may record temporal and spatial variability in climatic signals of the past better than tree-ring width, we combined dendrochronological time-series analysis with the calculation of stem hydraulic properties derived from radial vessel features. We aimed to reconstruct the development and sensitivity of the hydraulic system over six decades and to identify climatic control of xylem anatomy for five co-existing broad-leaved diffuse- and ring-porous tree species (genera Acer, Fagus, Fraxinus and Quercus) across three sites covering a precipitation gradient from 548 to 793 mm. We observed a significant influence of the climatic water balance (CWB) on the vessel features of all species, but the time lag, magnitude and direction of the response was highly species-specific. All diffuse-porous species suffered a decline in vessel diameter in dry years, and increase in vessel density in dry years and the year following. However, F. sylvatica was the only species with a significant long-term change in anatomical traits and a significant reduction in potential hydraulic conductivity (Kp) after dry winters and in dry summers, accompanied with the largest long-term decline in tree-ring width and the largest growth reduction in and after years with a more negative CWB. In contrast, the comparison across the precipitation gradient did not reveal any significant vessel-climate relationships. Our results revealed considerable plasticity in the hydraulic system especially of F. sylvatica, but also evidence of the drought-sensitivity of this species in accordance with earlier dendroecological and physiological studies. We conclude that the long-term reconstruction of hydraulic properties can add substantially to the understanding of the acclimation potential of different tree species to climate change.


2021 ◽  
Author(s):  
Landen Gozashti ◽  
Russell Corbett-Detig ◽  
Scott W Roy

Reproductive proteins, including those expressed in the testes, are among the fastest evolving proteins across the tree of life. Sexual selection on traits involved in sperm competition is thought to be a primary driver of testes gene evolution and is expected to differ between promiscuous and monogamous species due to intense competition between males to fertilize females in promiscuous lineages and lack thereof in monogamous ones. Here, we employ the rodent genus Peromyscus as a model to explore differences in evolutionary rates between testis-expressed genes of monogamous and promiscuous species. We find candidate genes that may be associated with increased sperm production in promiscuous species and gene ontology categories that show patterns of molecular convergence associated with phenotypic convergence in independently evolved monogamous species. Overall, our results highlight possible molecular correlates of differences in mating system, which can be contextualized in light of expected selective pressures.


2019 ◽  
Vol 48 (3) ◽  
pp. 417-425
Author(s):  
Md Khayrul Alam Bhuiyan ◽  
Md Akhter Hossain ◽  
Abdul Kadir Ibne Kamal ◽  
Mohammed Kamal Hossain ◽  
Mohammed Jashimuddin ◽  
...  

A study was conducted by using 5m × 5m sized 179 quadrates following multistage random sampling method for comparative regenerating tree species, quantitative structure, diversity, similarity and climate resilience in the degraded natural forests and plantations of Cox's Bazar North and South Forest Divisions. A total of 70 regenerating tree species were recorded representing maximum (47 species) from degraded natural forests followed by 43 species from 0.5 year 39 species from 1.5 year and 29 species from 2.5 year old plantations. Quantitative structure relating to ecological dominance indicated dominance of Acacia auriculiformis, Grewia nervosa and Lithocarpus elegans seedlings in the plantations whereas seedlings of Aporosa wallichii, Suregada multiflora and Grewia nervosa in degraded natural forests. The degraded natural forests possess higher natural regeneration potential as showed by different diversity indices. The dominance-based cluster analysis showed 2 major cluster of species under one of which multiple sub-clusters of species exists. Poor plant diversity and presence of regenerating exotic species in the plantations indicated poor climate resilience of forest ecosystem in terms of natural regeneration.


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