Evolutionary History of the Butterfly Subfamily Satyrinae (Lepidoptera: Nymphalidae)

Evolutionary history of the butterfly subfamily Satyrinae (Lepidoptera: Nymphalidae) Carlos Antonio Peña Bieberach Department of Zoology Stockholm University 2009 Evolutionary history of the butterfly subfamily Satyrinae (Lepidoptera: Nymphalidae) Doctoral dissertation 2009 Carlos Peña Department of Zoology Stockholm University S-106 91 Stockholm Sweden © Carlos Peña, Stockholm 2009 Cover illustration: Lethe corbieri Nel, 1993 ISBN: 978-91-7155-810-7 2 Abstract I present an overview of the evolutionary history of Satyrinae butterflies (Lepidoptera: Nymphalidae). By using Bayesian and cladistic methods, I develop a phylogenetic hypothesis as a basis for studying the evolutionary history of the group. After estimating ages of origin and diversification for clades of interest, I show evidence for a radiation of a highly species- rich group of grass feeders in Satyrinae —the tribe Satyrini— which explains in part the high diversity of this group. The timing of diversification for Satyrini butterflies coincided with the spread of grasses throughout the globe, which was followed by spread of the butterflies and colonization of new emerging habitats made available by the change in global climate during the Oligocene that facilitated the spread of grasses. Such a dispersal of Satyrinae was the result of a habitat shift from closed, forested environments into open, grasslands and savannas, which became increasinly common since the Oligocene. Such dispersal of Satyrinae was facilitated by the appearance of geographic bridges that permitted ancestral migrations from the Palaearctic into North America and from North to South America, such as the continuous forest belt of Beringia (at 31 Mya and 14–10 Mya) and the temporary GAARlandia landspan (during 35–33 Mya). Thus, I show that the Satyrinae butterflies are such a highly diverse and distributed worldwide group of organisms thanks to many factors that were of crucial importance in their evolution. Intrisic factors such as evolution of adaptive traits and phylogenetic constrains, as well as exogenous contingencies such as climate change and geological events. Thus, in this thesis I show strong evidence that Satyrinae is so species- rich because they were able to feed on grasses, escape from living in dicotyledonous forests and start inhabiting grasslands and savannas. Key words: hostplant use, habitat shift, diversity, grasses, biogeography, phylogeny. 3 Contents Abstract 3 List of papers 5 1 Introduction 6 2 Status of Satyrinae 10 3 The radiation of Satyrini and phylogenetic methods 14 4 Evolution of hostplant use 15 5 Conclusions 17 6 Acknowledgments 18 7 Bibliography 19 4 PAPERS I-IV This thesis is based on the following papers, which will be refered to by their roman numbers (I-IV): I. Pena,˜ C., Wahlberg, N., Weingartner, E., Kodandaramaiah, U., Nylin, S., Freitas, A.V.L. and Brower, A.V.Z. 2006. Higher level phylogeny of Satyrinae butterflies (Lepi- doptera: Nymphalidae) based on DNA sequence data. Molecular Phylogenetics and Evo- lution 40: 29–39. II. Pena,˜ C. and Wahlberg, N. 2008. Prehistorical climate change increased diversification of a group of butterflies. Biology Letters 4: 274–278. III. Pena,˜ C., Nylin, S. and Wahlberg, N. 2009. The radiation of Satyrini butterflies (Nymphalidae: Satyrinae): a challenge for phylogenetic methods. Manuscript. IV. Pena,˜ C., Nylin, S., Freitas, A.V.L. and Wahlberg, N. 2009. Biogeographic history of the subtribe Euptychiina (Lepidoptera: Nymphalidae: Satyrinae). Manuscript. Papers I and II are reprinted with permission from the publishers, which own the copyrights: I: c Elsevier B.V. II: c The Royal Society 5 Evolutionary history of the butterfly subfamily Satyrinae 1 Introduction molecular evolution to estimate relative rates of mutation, and in conjunction with the use Butterflies are probably one of the most of fossils as calibration points, it is possible charismatic group of invertebrates for lay peo- now to estimate ages of origin and diversifica- ple. Even though early interest in butterflies tion for virtually all living organisms. Some started as a mere “stamp collecting” hobby ac- studies, however, have drawn criticism for us- tivity, the massive collections gathered during ing molecular clock techniques without taking the late XIXth and beginning of XXth cen- into account uncertainty of the ages of fossils turies by wealthy individuals, with the help of that are used for calibration (Graur & Mar- paid collectors scattered throughout the world, tin, 2004). Graur & Martin (2004) issued a eventually ended up forming the most impor- strong reminder of how the results are badly tant scientific collections of butterflies in the affected when not including uncertainty in the world (e.g. the famous Walter Rothschild’s analyses —measured as standard deviation— collection at the Natural History Museum, especially for secondary and tertiary calibra- London). Although interest in butterflies was tion points. considered as a pastime at the time, there was Placing butterfly lineages in a temporal a strong scientific motivation to describe taxo- framework is vital for understanding major nomically as many species as possible. As an evolutionary events undergone by this group example, one of the most prolific describers of organisms, such as vicariant events, dis- of butterfly taxa, Hans Fruhstorfer, produced persal into new landmasses, and colonization an estimate of more than 5000 butterfly names and shifts of hostplants. Until recently, a great (Lamas, 2005). In time, due to the vast amount number of biogeographic studies on butterflies of knowledge gathered on this group, butter- have focused on using geological events to in- flies came to be regarded as model organisms fer ages of origin for butterfly groups (Vilo- for studies on evolutionary biology (Boggs ria, 2003; Braby et al., 2005). The advent of et al., 2003). However, important events in molecular methods have opened the possibly butterfly evolution, like the temporal and spa- of using a new source of information in bio- tial origin of major lineages, are just being re- geography. cently explored (Braby et al., 2005; Wahlberg, One way to understand nature is by study- 2006; Wahlberg & Freitas, 2007). ing the processes and factors that shaped the A troublesome issue is the age of origin planet’s current biodiversity. By using but- of all butterflies. The oldest butterfly fossil terflies as model organisms, several hypothe- —from a meagre fossil record— is just 48 ses have been proposed in order to explain My old (Kristensen & Skalski, 1999), which the diversity of several groups. Butterflies seems a relatively recent origin of butterflies are very dependent on their hostplants and when compared with that of their hostplants, since there is an intimate ecological relation- the angiosperms, that appeared between 180– ship where butterflies and plants have to ad- 140 Mya (Bell et al., 2005). The advent of just to their mutual adaptations and counter- molecular methods, and especially progress in adaptations, it has been hypothesized that co- developing cheap and quick DNA sequencing evolution may explain their diversity (Ehrlich techniques, has permitted the use of models of & Raven, 1964). By comparing estimated 6 Evolutionary history of the butterfly subfamily Satyrinae ages for butterflies and hostplants, it is pos- Likelihood (ML) and Bayesian Inference (BI), sible to rule out a coevolutionary scenario are approaches where more a priori knowledge if there is no evidence for contemporane- on the set of characters is used by employ- ous speciation events (Lopez-Vaamonde et al., ing models of character evolution. ML esti- 2006). Janz et al. (2006) show that interac- mates the probability of how well the data will tions between butterflies and their hostplants be explained by a phylogenetic tree (Felsen- produce diversification by expansions and spe- stein, 2004), while BI estimates the probabil- cializations of the hostplant repertoire. In the ity of how well a phylogenetic tree will be ex- megadiverse Neotropical region, there is evi- plained by the data (Huelsenbeck et al., 2001; dence for altitudinal speciation across a verti- Brooks et al., 2007). ML needs to calculate cal gradient of elevation in the Andes. It ap- each possible tree that can be derived from pears that taxa originate in montane habitats the data, according to the selected model of while their older relatives remain in the Ama- character evolution, in addition to calculations zonian lowlands (Hall, 2005; Whinnett et al., of branch lengths for each different topology 2005). These attempts to explain diversity are (Huelsenbeck & Rannala, 1997). BI is often heavily dependent on having a good degree of preferred over ML due to the use of “short- knowledge of the evolutionary history of the cuts” by employing the Markov Chain Monte groups under study. Carlo algorithm (MCMC) that permits search- In order to study the evolutionary history of ing over a smaller number of trees accord- any group of organisms, it is necessary to have ing to their posterior probability (Huelsenbeck a good understanding of their evolutionary re- et al., 2001). This allows BI to be less com- lationships, which can only be accomplished puter intensive and quicker than ML. While by constructing strong phylogenetic hypothe- these three methods are widely used, they are ses for our study groups. There are two pre- not exempt of criticism. MP is affected by viously hostile major camps in phylogenetic long branch attraction artifacts (Felsenstein, practice, the traditional cladistic

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