Correspondence were made by Lynch Alfaro et al. on 19 September 2014, immediately after the accepted version of this manuscript was sent to the authors on 18 September 2014. doi:10.1111/jbi.12448
Competing paradigms of Amazonian diversification and the Pleistocene refugium hypothesis ABSTRACT Evidence from butterflies and birds suggests that most extant Amazonian species arose during the Pleistocene (< 2.6 Ma). If these speciation events share common, extrinsic causes, their explanation probably involves climate-driven biogeographical shifts, because the major orogenic events shaping the biogeography of the Neotropics were over by then. In the light of these observations, criticisms of the Pleistocene refugium hypothesis are examined. Keywords Amazonia, crown ages, Neogene, Neotropics, Pleistocene, Quaternary, refuge hypothesis, tropical diversity. When we talk about ‘biodiversity’, most often ideas are framed in terms of the numbers of extant species in a given area (cf. Gaston, 1996; Mora et al., 2011). There are two different ways to pose the question of when this diversity arose. From a proximate perspective, most extant species are thought to be only a few hundred thousand to a few million years old (Hoorn et al., 2011), an estimate corroborated by evidence from Neotropical butterflies and birds (Garz on-Ordu~ na et al., 2014; Smith et al., 2014), and so one may enquire about processes and mechanisms acting during that time period to account for the origins of living species. From the perspective of deeper time, one can also ask questions about the ages of origin and temporal patterns of diversification (or impoverishment) of various clades through evolutionary history, noting of course, that ‘diversification’ of more inclusive taxa is a process that takes place through time, not an event to which a single date can be attached. Scientists interested in these differing temporal aspects of Neotropical Journal of Biogeography 42, 1349–1363 ª 2015 John Wiley & Sons Ltd
diversity and the mechanisms invoked to explain them have been described as holding ‘two paradigmatic and mutually exclusive options’ (Rull, 2013). As systematists and biogeographers, we are interested in general explanations of shared biotic distributional patterns in time and space. The empirical question asked in Garz on-Ordu~ na et al. (2014) was simply: did a considerable number of extant butterfly species in the region diverge from their sister taxa in the Pleistocene? According to our results, the answer is yes. That does not mean, as Rull (2014) correctly pointed out, that said speciation events occurred as a result of allopatric refugial vicariance. Although our title stated that timing of divergences is consistent with the Pleistocene refugium hypothesis (PRH), we did not intend to suggest in our paper that correlation is equivalent to causation. Thus, we agree with Rull (2014) that ‘demonstrating Pleistocene speciation is not the same as supporting the refuge hypothesis’. In fact, our strongest claim regarding the PRH was only that it ‘cannot yet be ruled out as an explanation of Amazonian species diversity’ (Garz on-Ordu~ na et al., 2014, p. 1636). We simply suggested that the PRH remains viable and should not be ‘abandoned’, challenging the belief, stemming from widely cited articles by Colinvaux et al. (2000), Hoorn et al. (2010) and others, that the PRH has been rejected as false or unnecessary to contribute to the explanation of patterns of Neotropical diversity. Our aim was to restore balance to the discussion on the timing of speciation in the Neotropical lowlands and to question the conventional wisdom that the PRH is necessarily defunct. The PRH does not preclude the possibility, but rather depends upon the historical certainty, that a diversity of plants and animals were present in the Amazon Basin prior to 2.6 Ma. Thus, Rull’s (2014) suggestion that we adhere to one of two ‘alternative paradigms’, at least in the sense of mutually exclusive explanations for Amazonian diversity, seems misplaced. There are four different types of arguments against the PRH. First, the ‘alternative paradigm’ espoused by Moritz et al. (2000), Behling et al. (2010), Hoorn et al. (2010) and others, which states that most or all of the ‘diversity’ in Amazonia was already present prior to the Pleistocene, and therefore the PRH is unnecessary to explain it. One of the central points of our paper was that such conclusions are often biased
by equating ‘diversification’ with the crown ages of clades (the age of the common ancestor of extant members of the group), which overestimates the divergence times of said clades’ constituent taxa. Perhaps, because our focus is on extant biodiversity while others are concerned with ‘total biodiversity’ (i.e. model-based extrapolations of how many species might have existed at various times in the past), the disagreement is merely semantic. Regardless, it is self-evident that the age of origin of a clade is not necessarily the same as the age at which it became ‘diverse’ (Rull, 2008, 2011), and that because the circumscription of a crown group is arbitrary, its estimated age is also arbitrary. For example, the average age of ithomiine butterfly genera is 16.2 Myr; the average age of ithomiine subtribes is 21.2 Myr; and the timing of divergence of ithomiines from their sister taxon is 45.7 Ma (Wahlberg et al., 2009). Which of these is the most pertinent ‘age of diversification’ for the group? It is possible, based on speciation models and molecular clocks, to develop quantitative scenarios of speciation rates through time that might avoid the arbitrariness of crown group ages (cf. Rabosky, 2006, 2014). Our less assumption-laden approach inferred the ages of extant species (the basic units of biodiversity) from uncorrected pairwise sequence divergences. If many (or most, cf. Hoorn et al., 2011) speciation events giving rise to the extant biota took place in the Pleistocene, as our butterfly data (as well as a recent meta-analysis of birds by Smith et al., 2014) suggest, then the argument that ‘diversification of most animals and plants occurred well before the onset of climate oscillations in the late Neogene’ (Antonelli et al., 2010, p. 389) is false: regardless of when their clades evolved or how diverse they may have been in the past, the diversity of species that live in Amazonia today is mostly of Pleistocene origin. Second is the argument that there were no Pleistocene refugia, based on fossil pollen samples. As noted by us and others (e.g. Behling et al., 2010), a small number of cores, drawn from lacustrine and alluvial fan sediments scattered around the Amazon Basin and representing only the most recent 60,000 years (2.5%) of the Pleistocene, is not representative of the spatial and temporal diversity of the region. Indeed, one might expect to find aquatic depositional environments such as lakes and rivers surrounded by remnant forest patches or gallery forests, even if the rest of
Correspondence Amazonia were more arid, and given that pollen dispersal may be quite spatially limited (Bateman, 1947), the pollen deposited in such environments could be representative of the immediately local flora and misleading with respect to more distant surrounding vegetation types (Hooghiemstra & van der Hammen, 1998). Furthermore, pollen cores from Laguna Pata, one of the key sites invoked as evidence for Pleistocene Amazonian forest continuity, have lately been re-examined and found to indicate a ‘significantly drier climate during the Last Glacial Maximum’ (D’Apolito et al., 2013, p. 140) – a pattern that is consistent with PRH predictions, although the site falls within a predicted forest refugium (Hooghiemstra & van der Hammen, 1998). Numbers, sizes and locations of hypothetical refugia remain poorly understood, but to suggest the abandonment of the PRH altogether on the grounds of the available pollen core evidence seems premature. Third is the suggestion that alternative vicariant biogeographical hypotheses such as riverine barriers and marine incursions may also explain Pleistocene speciation (Nores, 1999; Haffer, 2008). Recent interpretations of geological evidence (Campbell et al., 2006; Garzione et al., 2008; Hoorn et al., 2010; Hovikoski et al., 2010; Latrubesse et al., 2010; Nogueira et al., 2013) indicate that most orogenic phenomena had ended and that major Amazonian physiographic features such as mountain ranges and large river systems were more or less in their current positions between the late Miocene and late Pliocene. Thus, while they were undoubtedly important in the allopatric diversification of taxa during earlier times, such events could not play a role in vicariant speciation events occurring during the Pleistocene. Again, a central result of our paper is that the timing of speciation events we observed is not consistent with these alternative vicariant mechanisms. Rull (2014) listed two other vicariant hypotheses that are compatible with Pleistocene-age divergences: the canopy-density hypothesis (Cowling et al., 2001) and the disturbance–vicariance hypothesis (Colinvaux, 1993). As noted by Haffer (2008), the former is simply a less stringent version of the PRH sensu stricto, with dry forest instead of savanna separating refugia, and the latter emphasizes cooling rather than drying as the climatic agent of biotic shifts and changes. From our perspective, these hypotheses all operate in a functionally similar manner as climate-based drivers of
vicariant biotic distributions and are not distinguishable from one another with available data. Thus, we agree with Haffer (2008) that they represent variations on a common theme and consider them all potential mechanisms that could produce Amazonian refugia. Fourth is the rather nihilistic argument that there is no single explanation for Amazonian diversity, and that it is naive to seek such a holy grail. This comes in various forms, ranging from ecological selectionist arguments that each species evolved in response to biotic and abiotic stimuli in its environment in its own way, to more general exhortations that multiple explanatory hypotheses to explain Pleistocene diversification exist and should be investigated. As Rull (2013, p. 418) stated, ‘the high physiographic, environmental and biotic heterogeneity of the Neotropics, together with the long history of palaeogeographic reorganizations and palaeoclimatic changes (Hoorn & Wesselingh, 2010), precludes [sic] any generalization from selected case studies and particular regions’. Given the millions of species that occur in Amazonia, there is doubtless no one-sizefits-all explanation for Neotropical diversity. But are there no general patterns and processes that can be inferred? The original evidence of congruent distributions among clades of butterflies, birds, frogs, trees and other taxa (Haffer, 1969; Prance, 1973; Brown, 1979; Hall & Harvey, 2002) suggests, to the contrary, a tantalizing emergent pattern that could be fruitfully explained by a common, extrinsic vicariant mechanism. As Haffer (2008, p. 920) said, ‘ecological factors do not contribute to an understanding of the historical problems of the origin of species in Amazonia’. Rull (2013, 2014) emphasized the existence of mutually exclusive explanatory paradigms for Amazonian diversity, and criticized us for assuming that Pleistocene speciation must follow the rules of the PRH without providing all the evidence necessary to support such a conclusion. on-Ordu~ na et al. While the data from Garz (2014, p. 1633) are limited to the temporal aspect of the PRH, so were our conclusions: ‘Our findings with butterflies are consistent with the temporal predictions formulated by the PRH’. We remain committed to the idea that if taxa speciated in the Pleistocene, then a component of the explanation of those events is likely to be changes in environmental conditions related to climate, as the PRH predicts.
The replacement of the PRH with predominantly Neogene alternatives may be seen as a Kuhnian paradigm shift, influencing authors such as Smith et al. (2014) to reject the possibility of Pleistocene vicariance out of hand, but that agenda has been supported by conflation of generic or tribal crown ages with ‘ages of diversification’, and by extrapolations from pollen cores of rather ambiguous pertinence. Our results, as well as those of Smith et al. (2014), and, indeed, the general assumption of Hoorn et al. (2011), suggest that any paradigm that rejects Pleistocene speciation as a significant component of Amazonian diversification is incomplete. It is our opinion, based on the evidence reviewed above, that: (1) shared patterns of biotic distribution exist in Amazonia that can be parsimoniously interpreted as the results of vicariance; (2) speciation of many of the taxa involved occurred in the Pleistocene; and (3) Pleistocene climatic fluctuations and resultant shifts in biotic distributions provide a parsimonious causal explanation for those events – particularly in the absence of other general explanatory hypotheses. Given these tenets, we remain openminded to alternative explanations, as any empirical scientist ought to be. n - O r d u n ~a * † , Ivonne J. Garzo Jennifer E. Benetti-Longhini and Andrew V. Z. Brower Evolution and Ecology Group, Department of Biology, Middle Tennessee State University, Murfreesboro, TN, USA *E-mail: [email protected]
† Current address: California State Collection of Arthropods, California Department of Food & Agriculture, Sacramento, CA, USA
ACKNOWLEDGEMENTS We are grateful to George Benz for proofreading and discussion. Alexandre Antonelli and two anonymous referees provided thoughtful criticism on two drafts of the manuscript. This paper discusses the research undertaken through a collaborative grant, Dimensions US-Biota-S~ao Paulo: Assembly and evolution of the Amazon biota and its environment: an integrated approach, supported by the US National Science Foundation (NSF DEB 1241056), National Aeronautics and Space Administration (NASA), and the Fundacß~ao Journal of Biogeography 42, 1349–1363 ª 2015 John Wiley & Sons Ltd
Correspondence de Amparo a Pesquisa do Estado de S~ao Paulo (FAPESP Grant 2012/50260-6).
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Editor: Brett Riddle doi:10.1111/jbi.12539
How to define nativeness in organisms with high dispersal capacities? A comment on Essl et al. ABSTRACT Essl and colleagues documented worldwide invasion patterns in bryophytes, which so far have been neglected in invasion biology. In the absence of historical evidence, Essl and colleagues used criteria such as anomalous geographical distribution, preference for disturbed habitats, and indirect associations with some means of human transport as criteria to identify aliens. Because bryophytes exhibit high long-distance dispersal capabilities, disjunct distribution patterns are, however, the rule rather than the exception in the group. In our opinion, none of the previously proposed criteria to characterize aliens can be satisfactorily applied to groups like bryophytes, for which historical and fossil records are extremely scarce. We suggest that, in order to validate the conclusions of Essl and colleagues, further taxonomic and phylogeographical studies are needed. This is especially true for island floras, for which recent critical taxonomic work and updated checklists, which compose the primary source of information for biodiversity, are largely missing. Keywords Bryophytes, genetic diversity, genetic structure, invasive species, long-distance dispersal, nativeness. Invasive species are increasingly viewed as a significant component of global change and one of the major drivers of current biodiversity loss (Didham et al., 2007). In this context, nativeness has become the sine qua non invoked by many management policies, plans and actions to justify intervening on prevailing ecosystem processes (Chew & Hamilton, 2011). Although the distribution of alien species
urgently needs to be documented for risk assessments, such information remains scarce in some geographical areas and taxonomic groups (Vila et al., 1999). In particular, although the socio-economical and ecological impact caused by bryophyte invasions is minor compared with other taxonomic groups, alien bryophytes threaten habitats that are often of high conservation relevance, affecting other cryptogams, but also invertebrates, vertebrates, and vascular plant seedlings (Essl et al., 2014a). Based on a spatial analysis of the distribution of alien bryophyte species worldwide, Essl et al. (2014b) concluded that ‘bryophyte invasions exhibit marked biogeographic patterns on a global scale [. . .], with islands being clearly more prone to invasion’ (p. 9), ‘regions in the Southern Hemisphere have higher numbers of naturalized bryophytes’ (p. 1), and that ‘naturalizations occur more frequently in regions of the complementary hemisphere than in regions of their native hemisphere’ (p. 1). These findings raise intriguing questions about the historical, evolutionary and ecological mechanisms underlying these patterns. The distinction between native and introduced biotas presents, however, unique challenges (Bean, 2007). Comparative analyses using information previously published in floras and checklists, therefore, ‘crucially depend on the quality of assessment of particular species with respect to their taxonomic identity, time of immigration and invasion status’ (Pysek, 2003, p. 499). The distinction between native and introduced plants and animals is especially problematic in organisms with high long-distance dispersal capacities (Bean, 2007) and for which, like bryophytes, historical records are mostly lacking. Here, we reappraise the problem associated with the criteria that can be employed to identify alien species in highly mobile organisms. As pointed out by Essl et al. (2014b), direct evidence of introduction is available only for a limited number of bryophytes. Essl et al. (2013, 2014a,b) hence used criteria, such as the lack of historical records, anomalous geographical distribution, preference for disturbed habitats, and association with some means of human transport, to define alien species. Both experimental (L€ onnell et al., 2012, 2014) and phylogeographical (e.g. Sz€ ovenyi et al., 2012; Lewis et al., 2014; and references therein) studies have, however, demonstrated the high
long-distance dispersal capacities of bryophytes. Using spore-trapping experiments, Sundberg (2013) estimated that about 1% of the regional spore rain has a transcontinental origin. Disjunct distribution patterns are, therefore, the rule rather than the exception in bryophytes (Medina et al., 2011), challenging the use of such a criterion for identifying aliens. The disjunct distribution criterion led Essl et al. to qualify taxa with striking range disjunctions, such as the moss Syntrichia bogotensis and the liverwort Plagiochila retrorsa, which are primarily distributed in the Neotropics, as alien species in Macaronesia. Approximately 3.5% of the Macaronesian mosses and 8% of the Macaronesian liverworts exhibit range disjunctions between Macaronesia and tropical areas that are identical to those exhibited by S. bogotensis and P. retrorsa (Vanderpoorten et al., 2011), and could therefore be assigned as aliens based on the disjunct distribution criterion. Such an assessment is, however, contradicted by two lines of evidence. First, P. retrorsa occurs in pristine laurel forest environments in steep north-facing slopes (Rycroft et al., 2001). Most of the disjunct species between the Neotropics and Macaronesia similarly occur in the same (macro-)habitat (Vanderpoorten et al., 2011). While alien species can sometimes also invade more or less pristine environments (Carter, 2014), they tend to primarily occur in disturbed habitats (Bean, 2007; Essl et al., 2013). Although occurrence in disturbed habitats does not necessarily point to an alien status (Hassel et al., 2005), habitat specificity for pristine environments does not point to an alien status either. Second, population genetic analyses on the Northeastern Atlantic bryophyte flora indicate that islands have played a key role as a stepping-stone for transoceanic migrants between tropical regions and Europe during the Pleistocene (Pati~ no et al., 2015). In our opinion, therefore, and apart from the very few cases, such as Campylopus introflexus, Orthodontium lineare and Lophocolea semiteres (Stieperaere, 1994; Hassel & S€ oderstr€ om, 2005), for which historical evidence is available, assigning an alien status to bryophyte species based on criteria such as the anomaly of the disjunction can be misleading. This is especially true in poorly known oceanic archipelagos, such as St Helena and even Hawaii, which lack a recent and critical evaluation of their bryophyte floras, but were identified by Essl et al. (2014a,b, Journal of Biogeography 42, 1349–1363 ª 2015 John Wiley & Sons Ltd