bs_bs_banner Botanical Journal of the Linnean Society, 2012, 169, 117–134. With 4 figures Radiations and key innovations in an early branching angiosperm lineage (Annonaceae; Magnoliales) ROY H. J. ERKENS1,2*, LARS W. CHATROU3 and THOMAS L. P. COUVREUR4 1Utrecht University, Institute of Environmental Biology, Ecology and Biodiversity Group, Padualaan 8, 3584 CH, Utrecht, the Netherlands 2Maastricht Science Program, Maastricht University, Kapoenstraat 2, 6211 KW, Maastricht, The Netherlands 3Netherlands Centre for Biodiversity Naturalis (section NHN), Biosystematics Group, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, the Netherlands 4Institut de Recherche pour le Développement (IRD), UMR-DIADE, 911, avenue Agropolis, BP 64501, F-34394 Montpellier cedex 5, France Received 2 August 2011; revised 30 September 2011; accepted for publication 22 December 2011 Biologists are fascinated by species-rich groups and have attempted to discover the causes for their abundant diversification. Comprehension of the causes and mechanisms underpinning radiations and detection of their frequency will contribute greatly to the understanding of the evolutionary origin of biodiversity and its ecological structure. A dated and well-resolved phylogenetic tree of Annonaceae was used to study diversification patterns in the family in order to identify factors that drive speciation and the evolution of morphological (key) characters. It was found that, except for Goniothalamus, the largest genera in the family are not the result of radiations. Furthermore, the difference in species numbers between subfamilies Annonoideae (former long branch clade) and Malmeoideae (former short branch clade) cannot be attributed to significant differences in the diversification rate. Most of the speciation in Annonaceae is not distinguishable from a random branching process (i.e. chance), and no special explanations are therefore necessary for the distribution of species richness across the major part of the phylogenetic tree for Annonaceae. Only for a small number of clades can key innovations be invoked to explain the elevated rate of diversification. © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 169, 117–134. ADDITIONAL KEYWORDS: adaptive radiation – rate shift – sister-group comparison – stochastic branching pattern – temporal method – topological method. INTRODUCTION Radiations have also been put forward as an impor- tant factor explaining species-rich clades at higher Biologists are fascinated by species-rich clades taxonomic levels, such as families (e.g. Davies et al., because their size is associated with evolutionary 2005; Couvreur et al., 2010), orders (e.g. Davis et al., success (Raikow, 1988). These clades are often 2005) or above (e.g. Magallon & Sanderson, 2001; thought to be the result of a radiation. Indeed, studies Wang et al., 2009). However, the term (adaptive) that invoke radiation as an explanation for the exist- radiation is often uncritically used for any historic ence of species-rich plant genera are numerous in the increase in species numbers (Skelton, 1993). Linder literature (e.g. Richardson et al., 2001; Cronn et al., (2008) defined the term radiation simply as the 2002; Rüber, Van Tassel & Zardoya, 2003; Beherega- increase in diversity in a lineage, and therefore all ray et al., 2004; Cieslak et al., 2005; Whittall et al., biological diversity results from radiations. However, 2006; Schuettpelz & Pryer, 2009; Valente, Savolainen this practice erodes the explanatory potential of the & Vargas, 2010; Duputié, Salick & McKey, 2011). term and partly results from the fact that the term *Corresponding author. radiation is still ill-defined (Sanderson, 1998). More- E-mail: [email protected] over, the causes of such a supposed radiation are © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 169, 117–134 117 118 R. H. J. ERKENS ET AL. often unclear. It is generally stated that a taxon has PROBLEMS WITH THE DEFINITION the built-in tendency to radiate and proliferate OF ‘RADIATION’ (perhaps because of some presumed key character or historical event) when, merely, it is observed in ret- Questions about the diversity of evolutionary groups rospect that it has done so (Raikow, 1988). No causal are questions about variation in speciation and relationship between the observed characters and the extinction (i.e. diversification rate), which leave their diversification of the group is established, making the signatures in the shapes of phylogenetic trees explanation rather speculative. This is unfortunate (Mooers & Heard, 1997). Dated phylogenetic trees because an understanding of the frequency, causes provide important insights into the tempo and mode and mechanisms underpinning radiations will con- of evolution of clades (Glor, 2010). If, in such a tree, tribute to the comprehension of the causes of biodi- many lineages arise in a short period of time, it might versity (Seehausen, 2007). be concluded that a radiation has taken place. However, this conclusion is highly dependent on the meaning of the vague concepts ‘many lineages’ and the definition of ‘a short period of time’ (Gittenberger, THE MEANING OF ‘RADIATION’ 2004). At lower taxonomic levels, the concept ‘many One of the definitions of radiation is ‘the evolution of lineages’ is often equated with ‘species rich’. This a relatively large, monophyletic group of species or term covers a wide range between, for example, 62 higher taxa within a relatively short period of time’ species of Camissonia Link in Onagraceae (Levin (adopted from Gittenberger, 2004). If, in addition, et al., 2003), 1000 species of Impatiens L. (Janssens character and/or ecological divergence occurs, et al., 2009) and 2000 species of Euphorbia L. Next to the radiation can be called adaptive, otherwise it is this, the scope of the ‘short time’ for a radiation to nonadaptive (Gittenberger, 1991; Sanderson, 1998; take place is equally broad. At a macroevolutionary Rundell & Price, 2009). The result of a radiation is scale, a radiation can take tens of millions of years a (sometimes large) difference in species numbers (Erwin, 2006). At a microevolutionary scale, the term between the radiating clade and its nonradiating radiation has, for instance, been applied to time sister clade. frames of ten million years in the case of Inga Mill. Differences in species numbers between lineages (Richardson et al., 2001), three million years for can arise for many reasons, such as chance, avail- finches colonizing the Galápagos islands (Grant & ability of (new) resources, absence of competitors or Grant, 1996) or 100 000 years in cichlid fishes (Ver- possession of key innovations (for an elaborate dis- heyen et al., 2003). cussion of these factors, see Brooks & McLennan, The comparison of sister groups redefines evolu- 2002; Sudhaus, 2004; Seehausen, 2007; Losos, 2010; tionary success (i.e. species richness) in terms of Yoder et al., 2010). Thus, biologically, the ancestors relative size rather than absolute size (Raikow, of a radiation can be regarded as relatively unspe- 1988; Slowinsky & Guyer, 1993), and rates of spe- cialized in the first three scenarios, whereas, in the ciation and extinction are examined in the context fourth case, they are specialized (Sudhaus, 2004) of their relative and not absolute ages (Raikow, and would constitute an adaptive radiation. ‘Adap- 1988). The use of sister groups therefore resolves tive’ is thus about character evolution and ‘radia- the two above-mentioned problems. Sister-group tion’ is about speciation (Brooks & McLennan, comparison is a useful tool for this because sister 2002). Lineage diversification (speciation and extinc- clades are monophyletic, comparable in most basic tion) and character diversification (morphological aspects of their biology (although they can be dif- and ecological) should therefore be decoupled ferent) and of the same age. This approach also (although, inference mistakes can arise if the eliminates rank-based and other taxonomic artefacts decoupled characters shaped the phylogeny under (Sanderson, 1998), eliminating any investigator bias study; Sanderson, 1998; Maddison, 2006). In a (Brooks & McLennan, 2002). If differences between radiation of species, many new taxa arise (e.g. flow- sister groups are found, there is evidence for differ- ering plants; Willis & McElwain, 2002), and a radia- ential rates of diversification in one group over tion of adaptations leads to the origin of many another (Brooks & McLennan, 2002; Losos & Miles, characters (for examples of adaptive radiations in 2002). Because the use of sister-group comparison is flowering plants, see Classen-Bockhoff et al., 2004). essential to radiation research, the definition of The net number of lineages arising from a radiation radiation will be extended and defined as ‘the evo- of adaptations is not important and adaptive radia- lution of a relatively large, monophyletic group of tions can therefore contain a relatively small species or higher taxa within a relatively short number of species (e.g. the adaptive radiation of 28 period of time, compared with closely related mono- species of Hawaiian silverswords; Schluter, 2000). phyletic (sister) groups’. © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 169, 117–134 ANNONACEAE RADIATIONS AND KEY INNOVATIONS 119 DIVERSIFICATIONS IN ANNONACEAE However, their focus was to test hypotheses that might explain diversification and distribution