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The Discordance of Diversification

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The Discordance of Diversification Molecular Ecology (2010) 19, 4046–4060 doi: 10.1111/j.1365-294X.2010.04788.x The discordance of diversification: evolution in the tropical-montane frogs of the Eastern Arc Mountains of Tanzania LUCINDA P. LAWSON*† *University of Chicago, Committee on Evolutionary Biology, 1025 E. 57th St., Culver Hall 402, Chicago, IL 60637, USA, †Field Museum of Natural History, Zoology Department, 1400 S. Lake Shore Dr., Chicago, IL 60605, USA Abstract Species with similar geographical distribution patterns are often assumed to have a shared biogeographical history, an assumption that can be tested with a combination of molecular, spatial, and environmental data. This study investigates three lineages of Hyperolius frogs with concordant ranges within the Eastern Afromontane Biodiversity Hotspot to determine whether allopatric populations of co-distributed lineages shared a parallel biogeographical response to their shared paleoclimatic histories. The roles of refugial distributions, isolation, and climate cycles in shaping their histories are examined through Hierarchical Approximate Bayesian Computation, comparative phy- logeography, and comparisons of current and past geographical distributions using ecological niche models. Results from these analyses show these three lineages to have independent evolutionary histories, which current spatial configurations of sparsely available habitat (montane wetlands) have moulded into convergent geographical ranges. In spite of independent phylogeographical histories, diversification events are tempo- rally concentrated, implying that past vicariant events were significant at the generic level. This mixture of apparently disparate histories is likely due to quantifiably different patterns of expansion and retreat among species in response to past climate cycles. Combining climate modelling and phylogeographical data can reveal unrecog- nized complexities in the evolution of co-distributed taxa. Keywords: Approximate Bayesian computation, comparative phylogeography, Eastern Arc Mountains, Ecological Niche Modelling, Hyperolius Received 14 April 2010; revision revised 24 June 2010; accepted 27 June 2010 responded in concert to the same vicariant events or Introduction share dispersal paths (Zink 2002; Zink et al. 2002). While island chains or continental mountain ranges Alternatively, co-distributed lineages may contain a often experience similar geologic and climatic regimes, variety of phylogeographical patterns implying that cur- their biological inhabitants do not necessarily share the rent communities are composed of lineages that have same evolutionary histories. These naturally fragmented suffered past extinctions and ⁄ or have significant differ- and spatially structured systems provide an opportu- ences in dispersal ability (Zink 2002; Zink et al. 2002). nity to investigate the patterns and processes of diversi- Through the use of molecular and spatial analyses, fication by comparing evolutionary histories across comparative phylogeography can test for shared vicari- multiple lineages. If phylogeographical structure is con- ance and dispersal histories among species and can gruent across reciprocally monophyletic groups, the interpret the influences of geologic, climatic, and spatial most parsimonious explanation is that faunas have variables on emerging species (Bermingham & Moritz 1998; Arbogast & Kenagy 2001; Zink et al. 2002; Hicker- Correspondence: Lucinda P. Lawson, Fax: 312 665 7754; E-mail: [email protected] son et al. 2006). Ó 2010 Blackwell Publishing Ltd COMPARATIVE PHYLOGEOGRAPHY OF MONTANE FROGS 4047 Vicariant fragmentation into allopatric daughter lin- Modelling or Environmental Envelope Modelling) to eages may result from a variety of geographical events determine community-wide and lineage-specific respon- including mountain-building (Ribas et al. 2007), changes ses to dry and wet climate conditions (Martinez-Meyer in river courses (Pereira & Baker 2004), continental et al. 2004; Elith et al. 2006; Phillips et al. 2006; Elith & breakup (Gamble et al. 2007), sea-level changes (Van- Graham 2009). dergast et al. 2007), or shifts in the distributions of suit- able habitat owing to climate change (Knowles 2000, Comparing scenarios of concordance ⁄ discordance 2001). Of these geographical events, climatically between lineages induced fragmentation of once continuous suitable hab- itat is believed to be a major driver of diversification in Shared evolutionary history leaves a mark on co-distrib- topographically rich landscapes (DeChaine & Martin uted taxa either in mutual phylogeographical relation- 2005; Epps et al. 2006; Shepard & Burbrink 2009). Dur- ships, concordance of lineage-splitting events, or a ing climate fluctuations, populations of species that clo- combination of the two. If the spatial relationships of sely track environmental conditions may experience phylogeographical structure and the timing of diver- alternating periods of isolation and connectivity as habi- gence events are concordant between species, then they tats scale and descend along elevation gradients in are assumed to share an evolutionary history and response to warming and cooling (Hamilton 1976; He- respond in concert to vicariant events (Fig. 2a—the witt 1996, 2004; Wiens & Graham 2005; Kozak & Wiens ‘Shared History Scenario’). If, however, phylogeographi- 2006). During climate cycles, the amount of reciprocal cal relationships are concordant but differ in the timing gene flow between discrete mountain blocks may be of lineage-splitting events, spatial relationships of occu- heavily influenced on the degree of isolation or connec- pied areas are probably the critical factor influencing tivity associated with each climatic condition (Hewitt diversification (Fig. 2b—the ‘Geographic Determinism 1996, 2004; Wiens 2004). Examining the coincidence of Scenario’). Such asynchrony could arise from differen- major climate fluctuations to the spatial divisions and tial dispersal abilities across forming barriers, responses lineage splitting events among distinct lineages pro- to different temporal events, or pseudocongruence vides insight into how climate cycles shape the phylog- (Cunningham & Collins 1994; Hunn & Upchurch 2001; eography of species. To investigate the impact of Upchurch & Hunn 2002). A third possibility is that climate cycles on the phylogeographical patterns of cur- phylogeographical topologies differ, yet timing of diver- rent species found in restricted habitats, I compare the gence events is simultaneous (Fig. 2c—the ‘Time-Con- phylogeographical patterns of three lineages of montane strained Scenario’). This scenario suggests that while reed frogs (Hyperolius) throughout the Eastern Arc the route of colonization may be variable, the expansion Mountains (EAM) of Tanzania (Fig. 1) and use Ecological and cessation of gene flow are temporally constrained Niche Modelling (ENM—also called Species Distribution (e.g., glacial cycles or global climate shifts). Finally, a km Fig. 1 Distribution of sampled localities U = H. mitchelli of three frog species on a map of East- 0 Q = H. spinigularis 300 ern Arc Mountains in Tanzania and J = H. puncticulatus Highlands of Malawi. Mountain blocks Kenya containing populations of these lineages are marked with letters and major areas within this semi-linear system are Q denoted by numbers. A UJ Mountain blocks UJ A: West Usambaras Tanzania Q C B 1 B: East Usambaras Q C: Nguru/Nguu UJ D: Uluguru E E: Rubeho J J D Q QU F: Malundwe G F J J 2 G-K: Udzungwa J Q I M: Malawi J H J U 3 Regions J K Area 1: Northen EA Area 2: Central EA FU Area 3: Southern EA Q Area 4: Malawian Highlands M (extend through Malawi) Malawi lake 4 Ó 2010 Blackwell Publishing Ltd 4048 L. P. LAWSON Fig. 2 Comparative phylogeography (a) (b) A A A A scenarios. a: Shared History, b: Geo- graphic Determinism, c: Time Con- B B B B strained, d: Random. Branch lengths C C C C proportional to time. D D D D Species 1 Species 2 Species 1 Species 2 (c) (d) A A A B C B C A D C D C B D B D Species 1 Species 2 Species 1 Species 2 lack of correspondence in either spatial or temporal pat- amphibian community (Poynton 2003). Floral and fau- terns would result if each lineage acts independently of nal diversification within the EAM is probably directly others or if extinction has been frequent and random related to changes in environmental conditions through (Fig. 2d is one possible example—the ‘Random Sce- time that repeatedly fragment continuous forests and nario’). Congruence and discordance between different produce complex landscapes of heterogeneous habitats portions of phylogeographical trees may also exist similar to those observed today. Paleoclimatic evidence resulting from a mixture of these four patterns. This from highland and lowland lake sediment and glacial study investigates the roles of vicariance, range expan- cores in the East Afromontane region show that while sions, climate cycles, and migration at the lineage and temperature and moisture levels on mountaintops community levels that explain the diversity observed remained relatively stable through major climate cycles today. (Marchant et al. 2007; Mumbi et al. 2008), intervening lowlands experienced dramatic oscillations between wet forests and dry grasslands (Ashley 2001; Vincens et al. Study species and area 2003; Osmaston & Harrison 2005; Trauth et al. 2005; The three lineages examined here are the sympatric Kiage & Liu 2006). These elevation-dependent climatic African montane reed frogs (Hyperolius) from the EAM histories resulted in repeated
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