domingo, marzo 22, 2009

Plant-Insect Horizontally Tranferred Interaction between Mirmecophyte Plants and Ants


Figure 1: hollow thorn Mesoamerican Acacia.

Following the idea of the proceses that allow inter-organims interactions to move from facultative to obligate, lets take a look at the amazing case of acacia trees and its Pseoudomyrmex ants asociates.

Among tropical plants, around 100 genera host specialized ant colonies in structures called “domatia” and in part of these cases, plants also provide these ants with food. Ants in this association exhibits intensive territorial and cleaning behavior over the plant. This has as a consequence the expulsion of other herbivores and their eggs, and the detachment of invasive vegetation and sometimes fungi as well. Thus this relationship has been described as mutualistic.

Extensive revision of this case has suggested that the trait making the interaction between myrmecophyte plants and ants obligatory is usually the formation of domatia (nesting structures) on the plant. Domatia usually are located on hollow stem and shoots, hollow thorns (like in the Figure 1), in leaf pouches, petioles or even on fruits. Additionally, some myrmecophytes present plant derived food rewards like food bodies and extrafloral nectar (EFN) (See Figure 2).


Figure 2: Extrafloral nectar producing structures (upper) and food bodies on acacia tree, visited by Pseoudomyrmex ants.

However, despite these plants and ants seems to be vitally dependent on such interaction, the mutualistic association, even for the ones considered obligate, is transferred horizontally: both partners reproduce independently and the association has to be established di novo in each subsequent generation.


Figure 3: Phylogenetic reconstruction of section from Acacia subgenus includying facultative (grey) and obligate ant interacting plants (orange), based on combined data matrix of chloroplast DNA markers, AFLP cluster analysis (from Heil et al. 2004).

Another trait that has been proposed as relevant of the establishment of obligate plant-ant association correspond to the extrafloral nectar production. Inside the subgenus Acacia, both non-myrmecophyte and myrmecophyte plants release extrafloral nectar (see Figure 3). But the details of how this trait is expressed make the whole difference. In non specialized plants extrafloral nectar secretion respond positively to mechanical damage, herbivory or to the exogenous application of 1mM solution of the plant hormone jasmonic acid (also involve in other plant-herbivory chemical responses). By the other hand, in general, specialized myrmecophytes exhibit a constitutive (and comparatively slow) nectar release, irrespectively of whether exogenous stimuli applied. Thus the attraction of non-specialized nectar feeders (like unspecialized ants) seems to be related to the plant herbivory response machinery in non-myrmecophytes plants with EFN production, while on myrmecophytes this trait continuously expressed. Moreover, nectar composition on facultative EFN producers has three main sugars: glucose, fructose and sucrose, while myrmecophyte plants lacks sucrose (Figure 4).



Figure 4: Chromatograms of relative abundance of sugars in the EFN from non specialized (left) and myrmecophyte acacias (from Heil et al. 2005). Peaks identified as G; glucose, F: fructose, S: sucrose. Insert on left of graph is invertase activity in the nectar for each plant expresed as ug glucose released per ul of EFN per minute.

This is the result of post-secretory hydrolysis of the nectar sucrose on the obligate ant-interacting plant due to invertase activity. Sucrose and other di and trisaccharides are identified as a highly attractive sugars for many non-specialized ants. In nectar choice experiments using non specialized ants and myrmecophyte specialized ants it has been demonstrated that the addition of sucrose to the nectar of the derived myrmecophyte acacia, had triggered the attraction of non specialized ants, that previously (without sucrose) will not be attracted to the nectar of these plants but to the non-myrmecophyte ones. Contrarily, specialized ants are significantly attracted to nectar without sucrose. Analysis of digestive enzymes on these ants has repeatedly demonstrated the lower activity of invertases in extracts of the digestive systems of Pseoudomyrmex specialized ants, while the facultative plant interacting ants from the same genus, P. gracilis, showed greater invertase activity, this specie can actually live independently of acacia trees. Thus, this suggest that the obligate horizontally transmitted Acacia-Ant association is also supported by the transference of the hydrolysis process to the host plant in the evolution of this tight plant-insect association.



Cristian Villagra


PS: Follow the link to see a video of this fascinating interaction from the documental series The Secret Life of Plants.



References:

Agrawal AA. 1998. Leaf damage and associated cues induce aggressive ant recruitment in a neotropical ant-plant. Ecology 79: 2100–2112.

Heil M, Greiner S, Meimberg H, Krüger R, Noyer J-L, Heubl. G, Linsenmair KE, Boland W. 2004. Evolutionary change from induced to
constitutive expression of an indirect plant resistance. Nature 430: 205–208.

Heil M, Rattke J, Boland W. 2005. Post-secretory hydrolysis of nectar sucrose and specialization in ant/plant mutualism. Science 308:560–563.

Heil M. 2008 Indirect defence via tritrophic interactions. New Phytologist 178: 41–61.


martes, marzo 03, 2009

Homeosis de dedos de dinosaurios: Cuando la evolución predice las posibilidades del desarrollo

En el desarrollo del ala de las aves, es patente que los dedos se desarrollan a partir de primordios cartilaginosos que se convierten en los dedos 2,3 y 4 (indice, medio, y anular) en otros amniotos. Incluso se puede observar transitoriamente una pequeña condensación cartilaginosa anterior que sería un vestigio del dedo 1 (pulgar) 

Sin embargo, el registro fósil documenta con detalle la transición de dinosaurios terópodos a aves, y en este caso nos cuenta una historia completamente distinta, ya que en esta transición los dedos 4 y 5 (anular y meñique) se hicieron más pequeños y desaparecieron, quedando sólo las morfologías de los dedos 1,2 y 3. 

Para explicar esta peculiar situación, Wagner y Gauthier (1999) hipotetizaron que había ocurrido un desplazamiento homeótico en serie en la evolución del linaje de las aves, tal que los dedos 1,2, y 3 pasaron a desarrollarse de los primordios 2, 3, y 4. Esto implicaba asumir que al correrse la identidad de los digitos, el primordio que normalmente se desarrolla en el dedo 1 quedó "sin identidad" y que en esta posición "vacante" se desarrolla una condensación "truncada". Este evento podría coincididir con la pérdida del dedo 4, ocurrida hacia el origen de los dinosaurios tetanuros, "C" en la figura de abajo. A es Alligator, B es un dinosaurio temprano Coelophysis.


Tomado de Vargas y Wagner 2009

Hubo quienes rechazaron esta hipótesis ya que implicaba un cambio que no tenía ninguna "ventaja adaptativa"... 

Pese a desarrollarse a partir del primordio del dedo 2, el dedo anterior del ala tiene la morfología bifalangeal que es propia al dedo 1 de amniotos. Se ha demostrado además que en este dedo no hay transcriptos de los genes HoxD-11 y HoxD-12, tal como se observa sólo en el dedo 1 de la mano del ratón. También en crocodilia el dedo 1 carece de transcriptos de HoxD-11. Esto sugiere que el dedo anterior del ala  es un dedo 1.  Esta correspondencia de la transcripción de estos genes con el desarrollo de un dedo 1 bifalangeal se mantiene bajo una variedad de alteraciones moleculares-genéticas en ratón y pollo (amniotos máximamente distantes).

Ahora, un artículo en Evolution & Development ha demostrado que, por medio de la aplicación de cyclopamina en el ala del pollo, es posible producir de manera experimental un desplazamiento homeótico bastante similar al que se había inferido previamente para la evolución: dedos que normalmente se desarrollan de los primordios  2 y 3 ahora se desarrollan de los primordios 3 y 4. Esto es interesante porque antes sólo se habían obtenido de manera experimental transformaciones de dedos únicos, pero no así desplazamientos en serie de más de un dedo.  También es muy interesante que el primordio del dedo 2, al quedar vacante, se desarrolla como una condensacion vestigial, tal como se había inferido para la evolución de las aves. 
Fenotipo normal

Tratado con Cyclopamina, indicando condensación vestigial

 
Close-up de la condensación vestigial 


Referencia:
Vargas, AO y Wagner, GP. 2009. Frame-shifts of digit identity in bird evolution and Cyclopamine-treated wings. Evolution & Development 11(2): 163-9