Biological Journal of the Linnean Society, 2005, 84, 675-723. Towards a panbiogeography of the seas MICHAEL HEADS* Biology Department, University of the South Pacific, PO Box 1168, Suva, Fiji Islands Received 6 October 2003; accepted for publication 28 June 2004 A contrast is drawn between the concept of spéciation favoured in the Darwin-Wallace biogeographic paradigm (founder dispersal from a centre of origin) and in panbiogeography (vicariance or allopatry). Ordinary ecological dis­ persal is distinguished from founder dispersal. A survey of recent literature indicates that ideas on many aspects of marine biology are converging on a panbiogeographic view. Panbiogeographic conclusions supported in recent work include the following observations: fossils give minimum ages for groups and most taxa are considerably older than their earliest known fossil; Pacific/Atlantic divergence calibrations based on the rise of the Isthmus of Panama at 3 Ma are flawed; for these two reasons most molecular clock calibrations for marine groups are also flawed; the means of dispersal of taxa do not correlate with their actual distributions; populations of marine species may be closed systems because of self-recruitment; most marine taxa show at least some degree of vicariant differentiation and vicariance is surprisingly common among what were previously assumed to be uniform, widespread taxa; man­ grove and seagrass biogeography and migration patterns in marine taxa are best explained by vicariance; the Indian Ocean and the Pacific Ocean represent major biogeographic regions and diversity in the Indo-Australian Archipelago is related to Indian Ocean/Pacific Ocean vicariance; distribution in the Pacific is not the result of founder dispersal; distribution in the south-west Pacific is accounted for by accretion tectonics which bring about distribution by accu­ mulation and juxtaposition of communities; tectonic uplift and subsidence can directly affect vertical distribution of marine communities; substantial parallels exist between the biogeography of terrestrial and marine taxa; biogeo- graphically and geologically composite areas are tractable using panbiogeographic analysis; metapopulation models are more realistic than the mainland/island dispersal models used in the equilibrium theory of island biogeography; and regional biogeography is a major determinant of local community composition. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 84, 675—723. ADDITIONAL KEYWORDS: dispersal - distribution - ecology - marine - metapopulation - molecular systematics - spéciation - tectonics - vicariance. INTRODUCTION vicariance or allopatry over a region and there is no point centre of origin. Because Darwin-Wallace dis­ With the rise of interest in biodiversity and its persal is so widely assumed in studies of the marine regional structure over the last 15 years, biogeogra­ environment, this concept and alternatives are dis­ phy has been attracting more attention than ever. cussed below in some detail. Whittaker (1998) wrote Unfortunately, biogeographic methodology is still that: ‘Historical biogeography has lately been rather notoriously controversial. There are two main para­ polarized into two supposedly opposing camps, the digms used in studying and interpreting distributions: dispersalist and vicariance biogeographers, each traditional Darwin-Wallace dispersal (Darwin, 1859; concerned with how disjunct distributions arise.’ How­ Wallace, 1860, 1876; Matthew, 1915), in which taxa ever, the topic of the debate is rather more general evolve at a point centre of origin and attain their than this - it is not just about disjunct distributions, range by physical movement out from there; and pan­ but about how any spéciation (and all other form- biogeography (Croizat, 1958, 1968a, b, 1975; Craw, making and taxon-making) occurs, whether disjunct Grehan & Heads, 1999; Crisci, Katinas & Posadas, or not. 2003; Llórente et al., 2003), in which taxa develop by Panbiogeographic methodology involves the com­ parative study of as many distributions of unrelated *E-mail: [email protected] taxa as possible and integration of these with tectonic © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 84, 675-723 675 676 M. HEADS history. It contrasts with methods used in dispersal one derived the centre of origin, that led to Croizat’s biogeography in which the focus is on the study group development of the generalized tracks/vicariance and its ecology, especially its means of dispersal (Wil­ approach. For example, authors such as Darwin son, 1991). Panbiogeographic methods have been used (1859), Matthew (1915), Darlington (1957), Frey to analyse distributions of reef fishes and marine mac­ (1993) and Briggs (2003a) have assumed that the most roalgae in the Pacific (Heads, 1983; Chin, Brown & advanced species occur at the centre of origin and out- Heads, 1991), marine and terrestrial organisms in compete the primitive ones which migrate away. In south-east Asia (McManus, 1985), and marine triclad contrast, other dispersalist authors, such as Mayr platyhelminths world-wide (Sluys, 1989). Hajdu (1942), Hennig (1966) and the modern phylogeogra- (1998) analysed sponge distributions in a paper titled phers (Avise, 2000), assume that the most primitive ‘Toward a panbiogeography of the seas’, and in a taxa occur at the centre of origin and it is the advanced recent volume dedicated to Croizat, Aguilar-Aguilar ones which have migrated away (‘Progression Rule’). & Contreras-Medina (2001) gave a panbiogeographic (Nelson, 2004, noted that ‘Hennig’s rule is now reborn analysis of the marine mammals of Mexico. - as if it were for the first time - within phylogeogra- phy.’) This is a fundamental split within the dispers­ alist school, but neither assumption is used in FOUNDER DISPERSAL, VICARIANCE AND vicariance cladistics (e.g. Platnick, 1981; Nelson, ECOLOGICAL DISPERSAL 2004) or in panbiogeography. Briggs (2000, 2003a) claimed that the pattern in C entres o f o rig in and th e ‘common -sen se ’ view which the ‘apomorphic’ species occur at marine cen­ OF DISPERSAL tres of origin has been ‘consistently displayed’ in the Darwin (1859) felt that each species begins by evolv­ Indo-West Pacific, but this is quite incorrect - a point ing at a point centre of origin from which it spreads centre of origin has been theorized countless times but out, and that the simplicity of this view ‘captivates the it has never been ‘displayed’ or demonstrated as exist­ mind’ (cf. Heads, 1985). Most subsequent authors have ing for any species, let alone being characterized by also been captivated by this concept. ‘apomorphic species’. For traditional dispersalists Ekman’s (1953) comprehensive and lucid book on such as Briggs, deducing which species are ‘primitive’ marine zoogeography is probably the single most and which are ‘advanced’ in a genus, and so which influential work in the field - a great deal of contem­ evolved from which, are important procedures. How­ porary work comprises timid variations on just a few ever, panbiogeography and cladistics agree that while of his themes. Ekman utilized Darwinian dispersal, characters might be primitive or derived, taxa are arguing, for example, that ‘Chance . plays a larger generally not. The species in a genus are alternative part in the possibilities of distribution for the fishes recombinations of characters, and the species are than for most other shelf animals’, and that ‘The derived from a common ancestor, not one from the longer the time the greater the part played by the so- other (Nelson, 2004). called chance factor, that is to say, the interaction of Despite his adherence to Darwin-Wallace dispersal, unknown factors . .’ He relied on currents as means as cited above, Veron (1995) concluded that ‘The fun­ of dispersal, and explained faunistic boundaries, such damental strength of Darwinian evolution, the most as his famous ‘East Pacific barrier’ (‘surmounted by universally accepted and fundamental concept of very few species’), as ‘barriers’ to dispersal. Nature the world has ever seen, is its all-encompass­ Veron (1995) argued that ‘Dispersion (migration), ing internal consistency . Yet the geographic basis the Achilles heel of vicariance, is of overwhelming of Darwin’s evolution, his centres of origin, have been importance in most corals’ and that ‘The presence of roundly rejected by most [coral] biogeographers’. Dar­ wide geographic disjunctures within the distribution win’s centres of origin theory, ‘the first of the major ranges of species are of great biogeographic interest theories of biogeography, is strongly refuted as a whole because they demonstrate the capacity ... of corals to by present knowledge of coral species . .’ What are disperse over long distances.’ Likewise, authors have the alternatives to a Darwinian ‘centre’? asserted simply that ‘Biogeography starts at the colo­ nizing event’ (Planes, 2002), and that island popula­ tions ‘have certainly experienced a founder effect V icariance and dispersal initially’ (Planes & Fauvelot, 2002). Veron (1995) con­ Scheltema (1995), a dispersalist, argued that ‘the cluded tersely that ‘Distribution patterns [in marine capacity for dispersal is not the sole condition which taxa] are the outcome of distribution by currents’. But contributes to the geographic distribution of benthic is this ‘common-sense’ view actually true? species . there are also ecological constraints . .’ In As George (1987) pointed out, it was