11
Kunga Choden
Bio -151 – Evolution
Research Paper
Evolution of Carnivorous Plants
Other than sunlight and water, plants require many different chemicals for proper growth and development. Over the course of their evolutionary history, different plants have evolved according to different selective environments. Thus, we are able to find plants in both cold areas such as the tundra or in hot places such as the desert; however, the form and function of these different plant groups differ. Hence, it is reasonable to theorize that carnivorous plants evolved in environments that lacked certain nutrients such as nitrogen and other essential metabolites. The extant carnivorous plants are descendents of the first ancient carnivorous plants that had successfully adapted to digesting small insects to fulfill their nutrient requirements in stressful environments. We know that carnivorous plants trap insects and wait until the insects die and decay before they absorb the required nutrients. There are many different enzymes involved in these digestive processes. A biologist at any level is aware that the most valuable and limiting mineral element a plant requires is nitrogen. Thus, carnivorous plants must derive nitrogen from their prey. There are four types of traps in seed bearing carnivorous plants in the United States and Canada, which are closing traps, trap doors, pitfalls and flypaper, and they are further divided into two main groups: the first two traps are active and the later two are passive form of traps in carnivorous plants (Schnell, 1976). There are also many different variations of these types of traps in carnivorous plants. Therefore, we are confident that carnivory in plants evolved more than once.
Carnivorous plants are plants that catch or trap prey, absorb metabolites from their prey and utilize these metabolites in their growth and development (Adamec, 1997). Darwin first studied carnivorous plants in the summer of 1860 and was the first to publish a work covering carnivorous plants. In Insectivorous Plants, he points out that he was “surprised by finding how large a number of insects were caught by the leaves of the common sun-dew (Drosera rotundifolia) on a heath in Sussex” (Darwin, 1875). Darwin was also amazed by the number and size of insects (including small butterflies) caught by these plants. He was impressed by the complexity of the glands and leaves that trapped the insects and secreted various molecules to digest them. Darwin found out that the exterior tentacles were excited when one touched the glands, yet the repeated drops of falling water had no effect. Thus, he concluded that there must be selectivity and other mechanisms at play that controlled the inflexions in these carnivorous plants. Moreover, Darwin conducted various experiments with temperature and the introduction of different molecules such as salt and ammonia to see their effect and to understand the biological machinery that governs the physiological function of these carnivorous plants. Darwin’s pioneering work with carnivorous plants paved way for later experiments by other researchers on carnivorous plants. Darwin knew through his theory of natural selection that carnivorous plants had a selective advantage in their particular environments. There are many questions that surround the nature of carnivorous plants including their relationship to other plants, their prey, their phylogeny, the nutrients they absorb, the morphology of their structures and much more. This paper will study carnivorous plants in an evolutionary context covering all of the major characteristics that make carnivorous plants unique in the plant kingdom.
By the early 1940s, in Lloyd’s The Carnivorous Plants, the author had estimated there to be around 450 or more species of carnivorous plants. This number had increased to 600 species in the late 1990s (Adamec, 1997). A question that arises is whether these carnivorous plants went through a convergent or divergent evolution. Moreover, Lloyd discusses the existence of carnivorous fungi. Since fossils of carnivorous plants are not well-preserved, there are no records of any ancient carnivorous plants other than the extant ones.
Phylogeny
Through sequence and morphological analysis of various different genes and structures, we have found out that the ancestor of the first carnivorous plants were non-carnivorous angiosperms. Albert et al. derived a phylogeny of carnivorous plants by using “the plastid gene rbcL [which] encodes the large subunit of ribulose-1, 5-biphosphate carboxylase/oxygenase (RuBisCO), a prime enzyme in the Calvin-Benson cycle” (Albert et al., 2009). Their phylogeny showed that carnivorous plants displayed both homology and analogy in structural evolution. Therefore, one could see both convergent and divergent evolution patterns in the derived phylogeny. It is also understood from the phylogeny that carnivory is polyphyletic. For example, convergent evolution is observed between byblis and Drosophyllum; this is similar to the polyphyletic relationships drawn from angiosperms regarding C4 photosynthesis. From the phylogenetic study we are also able to conclude that the special structure of many of the carnivorous plants are homeotic and are likely to be products of different cell differentiation rather than de novo structures.
The conclusion that convergent evolution exists in carnivorous plants is also supported by Adams et al. 1977. The authors determine that three carnivorous pitcher plants, the Nepenthaceae, Sarraceniaceae, and Cephalotaceae, all belong to three distinctly separate orders – it is an amazing find since, “their basic morphology (both gross and microscopic)for performing the function of luring, capturing, and digesting insects is quite similar” (Adams et al., 1977). All of the three families possess some variation of the following structures: for luring they have nectar glands and toothed rim or directive hair; for capturing prey they possess ablative wax, smooth surfaces, directive hair and conductive funnel; and for digestion they have bacteria retentive hairs or digestive glands. It has been demonstrated in many different studies that carnivorous plants that were subjected to similar selection are found in similar substrates (soil high in moisture and acidity and low in nitrogen and other nutrients) (Adams et al. 1977). Therefore, the passive carnivory seen in these carnivorous plants from three distinct orders are a result of similar selection.
Carnivorous plants that share similar morphologies with a common origin have also been observed (Cameron et al.). In their study of snap-traps, the authors show that snap-traps in carnivorous plants evolved only once. The phylogenetic data was based on the sequence analysis from nuclear 18S and plastid rbcL, atpB, and matK genes. Their analysis concluded that Aldrovanda is sister to Dionaea, and that both are snap-trapping carnivorous plants. The authors also report a similar morphological similarity between the two groups such as the, “rapid transmission (6-17cm/s) of action potentials between excitable cells” used in the snap-traps. From their phylogenetic tree they also conclude that snap-traps of Androvanda and Dionaea had a common terrestrial ancestor that possessed flypaper-traps. It is also shown that pitfalls of pitcher plant genus Nepenthes also evolved from a flypaper-trapping ancestor. By looking at the non-carnivorous out-groups (such as Plumbago, Tamarix, Frankenia) that also posses structures and functions similar to carnivorous plants including multicellular glands that produce mucilage, salt or other compounds, they concluded that modification of these pre-existing structures and co-option of trigger hairs could have produced the first carnivorous fly-traps. Moreover, they report that in flooded areas, these carnivorous plants were able to capture prey and grow underwater. Thus, one can imagine these plants living in a permanently aquatic environment. Another study by Rivadavia et al. shows that close relationships can be derived between the multi-cellular hairs of Drosera and Aldrovanda and Dionaea. Furthermore, the origin of these unique hairs and glands of carnivorous plants are traced back to adhesive glands in Plumbaginaceae (Rivadavia et al., 2003). Their results suggest that the flypaper morphology of Drosera and the snap trap system of Dionaea and Aldrovanda were established early in the evolutionary history of these carnivorous plant taxa. The phylogenetic tree obtained through sequence analysis of various genes is further refined by looking at the chromosome number and diversity that were caused by aneuploidization and polyploidization, which might give rise to new species in the different carnivorous plant groups.
The Feeding Ecology
It has been shown that all carnivorous plants are able to digest both terrestrial and winged insects and uptake nitrogen, phosphorus, sulfur, potassium, calcium and magnesium from their prey (Adamec, 1997). In a study on subarctic carnivorous plant, lower rates of photosynthesis compared to non-carnivorous plants have been reported (Mendez & Karlsson, 1999). A weak correlation between nitrogen content and photosynthesis has been also demonstrated in the study. However, the authors also report that an increased rate of photosynthesis is possible as a result of obtaining essential nutrients through carnivory. They also show that the increased reproduction observed in carnivorous plants is an indirect consequence of increased photosynthetic capability through carnivory. Over the course of their evolution, carnivorous plants have developed varying dependence on prey for required nutrients. In some cases, carnivorous plants can digest the carbon from the decaying body of their prey. Hence, the possibility of seeing a heterotrophic carnivorous plant in the future is also possible.
Carnivorous plants capture prey of diverse orders including arachnids (Zamora, 1990). These carnivorous plants are both generalists and specialists. Their diet consists of a main prey and various other insects. By conducting experiments with mimic-traps, it has been shown that, “there does not seem to be a taxonomical selection in the diet” (Zamora, 1990). Prey selection is viewed as being dependent on size, which is directly related to the capturing mechanisms such as the stickiness of the mucilage on the flypaper traps. Therefore, evolutionary speaking these carnivorous plants have selected against smaller insects. In the future, the study of these carnivorous plants should pay special attention to the size of the prey and the adhesive system of the respective plant.
Carnivorous plants display highly adaptive features. One example is Nepenthes rafflesiana, which utilizes two pitchers. The high pitcher captures aerial prey and the low pitcher specializes in capturing ground prey. The differentiation of these two pitcher types might have some evolutionary significance. The species has evolved so that visual and olfactory stimuli are present in the high pitchers (low density of prey) and no such stimuli are detected in the lower pitchers (high density of prey and other insects). Contrary to the forms of prey discrimination found in Drosera and Sarracenia regarding UV patterns, these visual cues as mechanisms of prey attractions are not observed in Nepenthes (Joel et al., 1985). The reason proposed by the authors for the absence of these stimuli in the lower pitcher is that excessive holding of many prey and other insects can actually result in the death of the pitcher. They also suggest that carnivorous plants might also display mutualistic behavior since they don’t consume all prey that passes across the leaves of the plants.
Environmental effects
The effect of the environment on the success of carnivorous plants is significant, as mentioned earlier in the paper. The factors that contribute to the success of these plants concern the effect of certain parameters such as temperature, nitrogen, soil humidity and light. The availability of prey, which is most prevalent in the shadiest regions, also has a significant impact on the success of these plants (Alcala and Dominguez, 2003). Prey abundance is directly dependent on the environment; therefore, the success of carnivorous plants, prey availability and the environmental conditions are directly related to each other. Because different populations of carnivorous plants capture different prey, one can see a difference in the taxonomic composition of the prey and the prey actually captured by different carnivorous plants. Contrary to the other findings, Alcala and Dominguez 2003 state that no solid evidence supporting the capture of certain prey due to the color and smell of leaves has been established. Because the plants in the shadiest populations with high amounts of prey captured cannot take advantage of the high-nutrient environment, the authors suggest that carnivory cannot substitute for low levels of photosynthetic activity in these environments. The authors also make the claim that carnivory is adaptive only in nutrient-poor, well lit and moist environments. A tradeoff is observed between highly-lit areas with low prey, high temperature and dry soil, and one with high water and prey availability, but not well lit environments. Hence, different types of carnivorous plants are observed in these two different ecological niches, and the authors claim that intermediates of the two extreme conditions provide the most suitable habitat for the most successful carnivorous plants. If this is true, then one should be able to find the successful carnivorous plants in intermediate environments, and plants in the two extreme environments should demonstrate specialized form and function relating to that particular environment. This evolutionary strategy might also effect the interaction of these different types of carnivorous plants with their prey.
Some carnivorous plant such as Pinguicula vallisneriifolia have become specialized due to their unique environments such as rocky substrates and therefore are more successful in these environments than in nutrient rich soil (Zamora, 1997). The authors demonstrate that P. vallisneriifolia has therefore evolved to have a higher level of dependence on prey for nutrients than the soil. Thus, one might be able to find unique characteristics in the roots of these plants in regard to form and function compared to other carnivorous or non-carnivorous plants. Similar findings are also observed in studies done on two sympatric species of Drosera (Thum, 1976). Leaves of Drosera rotundifolia are found lying flat on the ground whereas Droserfa intermdia stands in an upright position. Thus, two microhabitats are established for these two closely related plants – one specializes in aerial traps whereas the other specializes in ground traps. These two different species also exist on different substrates. D. intermidia is often found on water, thus, not accessible for terrestrial arthropods, and D. rotundifolia is observed covered with moss and small bushes making it hard for aerial insects to land on it. These two sympatric species might have diverged due to disruptive selection. Also, the preference of different arthropods for the two different species might have also resulted in the establishment of these two distinct carnivorous plants in different ecological niches. The authors make the assertion that benefits of one year can carry on to the next year via the size of the winter bud in these plants. Consequently, the evolutionary selections for these microhabitats are under very strong selection.