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BUTTERFLIES in the LANDSCAPE Host Specialization, Niche Partitioning and Mimicry

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BUTTERFLIES in the LANDSCAPE Host Specialization, Niche Partitioning and Mimicry BUTTERFLIES IN THE LANDSCAPE Host Specialization, Niche Partitioning and Mimicry Honor’s Thesis (Trabajo de Grado) – Biology Universidad de los Andes - 2020 Daniel Fernando Faccini Otero Advisor: Santiago Madriñán [email protected] Resumen Este trabajo se divide en tres partes que pretenden dar respuesta a distintas preguntas. La primera busca responder la pregunta de “¿por qué los insectos herbívoros se especializan?” desde una perspectiva ecológica y fisiológica utilizando mariposas Heliconius silvestres como modelo de estudio. También se discute la posibilidad de que el proceso de especialización no sea un proceso adaptativo. En la segunda parte, se describe un nuevo caso de mimetismo batesiano y se propone un modelo mimético para las mariposas Riodinidae que tienen un fondo negro y tres bandas amarillas. Finalmente, la última sección propone un concepto nuevo para describir la relación, altamente dependiente, que se da entre insectos herbívoros especialistas y sus plantas hospederas a lo largo de la historia evolutiva: el bejuco filogenético. Summary This work divides into three parts that aim to answer different questions. The first one addresses the question, “why do insect herbivores specialize?” from an ecological and physiological perspective taking as case study Heliconius butterflies from a natural population. Yet, it is also considered the possibility that specialization could be a non- adaptative process. The second part proposes a novel mimetic model for the rare black and yellow Riodinidae believed to be Batesian mimics. Finally, the third part is the proposal of a new concept to describe the highly dependent relationship between specialist insect herbivores and their hostplants: the phylogenetic bejuco. Ecological and physiological patterns underlying host specialization in insect herbivores: Could it be a non-adaptative process? Introduction Insects are by far one of the most species-rich animal groups and among them, those that feed on plants seem to be more diverse than their related non-herbivorous groups (Stork, 2018; Wiens et al., 2015). Therefore, it is not surprising that early seminal papers such as Ehrlich and Raven (1964) already pointed out the utmost importance of plant-insect coevolutionary relationships in the understanding of insect diversity. Furthermore, crucial to this agonistic relationship is the phenomenon of specialization: most herbivorous insect species are restricted to feeding on a single family of plants even in highly diverse plant ecosystems such as tropical rainforests (Forister et al., 2015). Consequently, it seems to be necessary to understand why and how insects specialize to be able to explain the diversity of this fascinating group. Several hypotheses that pretend to explain why herbivorous insects specialize have been proposed such as the physiological efficiency hypothesis, the preference-performance hypothesis, the enemy-free space hypothesis and the neural constrains hypothesis. The first one states that specialist insects are physiologically adapted to the physical and chemical traits of their host and, therefore, they can outcompete generalists in the consumption of that particular plant (Dethier, 1954). The second one states that insects feed on the plants in which they perform better (i.e., preference is correlated with performance) (Gripenberg et al., 2010). The third one states that insects specialize to take refuge or to acquire chemicals to defend themselves from predators such as parasitoids (Singer, 2008). The fourth one states that, as insects have a limited cognitive capacity, they only will be able to discriminate between high-quality and poor-quality potential hosts if they specialize in a small subset of plant species (Bernays & Wcislo, 1994). Finally, another alternative explanation is specialization because of the classical niche partitioning to avoid competence with closely related species (Hutchinson, 1959). However, none of these hypotheses has received univocal support. The explanatory power of each hypothesis seems to be highly dependent on the studied taxonomic group or the experimental conditions. Nevertheless, the question “why do herbivorous insects specialize?” is divided into two very different questions: “why do insects eat plant species X?” and “why do insects eat only plant species X?”. Of the hypothesis explained earlier, only the neural constraint hypothesis and the physiological efficiency hypothesis address the latter question, while the others address the former. To tackle both questions, this investigation focuses on a well- studied model of specialist herbivores and their hosts: Heliconius and Passiflora. This system is particularly interesting because it includes both, monophagous and oligophagous species that feed upon the same set of chemically and morphologically diverse plant species (Benson et al., 1975; de Castro et al., 2018; J. Smiley, 1978; J.T. Smiley & Wisdom, 1985). Past studies of this system have concluded that the radiation of Heliconius occurred in the absence of phytochemical barriers as they may have an efficient detoxification system that allows them to eat almost any Passiflora plant (John T. Smiley, 1985; J.T. Smiley & Wisdom, 1985). However, some questions remain unanswered regarding these studies such as: why some Heliconius species do not develop on certain Passiflora species? (see also Waage et al. (1981))And why are some Passiflora species only eaten by a single Heliconius species? (see also (John T. Smiley, 1982)) Perhaps, the findings of Smiley and Wisdom (1985) do not demerit the importance of physiological explanations but are rather an invitation to explore the ecological factors that underlie the process of specialization in herbivorous insects. Overall, this study aimed to determine some of the ecological and physiological patterns that underlie specialization in herbivorous insects. To achieve this objective, no-choice diet experiments of Heliconius larvae were complemented with natural history observations of host and habitat preference. Finally, Heliconius data are complemented with data from Passiflora associated Alticini leaf beetles of the same community to make a conclusive remark regarding the possibility of specialization being a non-adaptative process. Methods Study site The study took place at a fragmented mountain forest at Colombia’s central cordillera in the town of Victoria, Caldas (1000 m AMSL) during the months of August-November. During this period, the months of August and the first half of September were dry with scarce rain while the latter months had daily rains. Five transects with variable longitudes (200m- 600m) and a three-meter width were delimited spanning different ecological conditions such as forest, forest border, and open habitat. During the delimitation of the transects, all Passiflora plants were localized, identified to species level, and georeferenced. Determination of preference Different combinations of transects were walked daily, for a total of 600 hour of sampling, except on rainy and extremely cloudy days in which butterfly activity was seriously diminished. All plants that were previously identified were scrutinized to find Heliconius eggs and leaf beetle adults. In the case of butterfly eggs, they were manually collected with the fingers, a unique identification number was assigned, the host plant was registered and finally, eggs were taken in a small recipient to a greenhouse where they were reared to an advanced instar that allowed certain taxonomic identification. Other Lepidoptera larvae and eggs were collected occasionally when found in the examination of the host plants. On the other hand, leaf beetles were assigned to morphospecies, and hostplant species were registered. For the posterior analysis of specialization, Lloyd (1967) mean crowding index was used to quantify specialization based on the number of observations (eggs for the butterflies and adults for the leaf beetles) for each insect species on each Passiflora. This index was preferred over more recent proposals such as Blüthgen et al. (2006) Kullback-Leibler distance because indexes based on whole network analysis seemed to be very sensitive to hyper-abundant species. Performance evaluation Collected eggs were taken to a greenhouse (Day: 26.8 ± 1.3°C, Night: 23.7 ± 1.3°C) in a 2 oz plastic container and a 1 cm piece of paper towel was added to raise humidity. The eggs were checked daily in the morning and the afternoon to register the hatching date and assign a Passiflora species to feed upon. As soon as hatching was registered, larvae were transferred to individual 16oz plastic containers with a small piece of wood to climb, a humid piece of paper towel, and a young leaf of the assigned plant. Once the larvae molted to the 3rd instar, the paper towel was removed, and older leaves were provided. As it was necessary that “same quality” leaves are provided to all the individual experiments, new leaves with no signs of damage or disease were collected daily from wild plants to feed larvae. When larvae pupated, the day of pupation was registered and after 24 hours (the time needed for the cuticle to harden) they were weighed on an electronic scale. After the pupae were weighed, they were re-adhered to the 16oz container lid and they were checked daily to register the adult emergence date. Finally, sex was registered, and adults were returned to the natural population or they were taken to a breeding cage to obtain eggs of known taxonomic identification for the experiments (some
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