Proximate sources of marine biodiversity

Authors


*John C. Briggs, 82-651 Sky View Lane, Indio, CA 92201, USA.
E-mail: clingfish@earthlink.net

Abstract

When temperature and other kinds of barrier divide formerly continuous populations and confine them to more restricted geographical areas, there is an evolutionary reaction that will, over time, result in the formation of endemic species. In such cases, an allopatric speciation process is considered to have taken place because reproductive isolation was caused by physical means instead of by natural selection. In contrast, when populations exist in a very high-diversity area and remain undivided by physical events, they exhibit a tendency to speciate by means of sympatry (or parapatry). This process, sometimes called competitive or ecological speciation, does involve reproductive isolation by means of natural selection. Populations that exist in geographical provinces bounded by physical barriers add to the overall diversity through the production of endemic species. This increase by species packing is relatively slow due to the very gradual tempo of the allopatric speciation process. Populations existing in centres of origin add to the general diversity through the production of species that are dominant in terms of their ability to spread over large parts of the world. It is proposed that such species are usually formed by sympatric speciation, a process that can be c. 20 times faster than species formation by allopatry. It is not suggested that sympatry is exclusive to centres of origin, nor that allopatry is confined to peripheral provinces. Both processes are widespread, but there do appear to be distinctive geographical concentrations. Considering that numbers of widespread species produced by centres of origin may eventually become subdivided by barriers, and thus give rise to descendants by allopatry, it is difficult to say how much of our present species diversity has come from one source or the other. Both speciation by sympatry from centres of origin and speciation by allopatry in peripheral provinces appear to be important sources of marine biodiversity.

Introduction

Over the Phanerozoic, species diversity, although it has shown considerable losses and gains, has continued to rise. Using palaeontological data on the rates of extinction, origin, and on the average longevity of marine animals, Sepkoski (1998) determined an approximate extinction rate of 2.5 species per year and an origination rate of 3.0 species per year. Therefore one should expect a historical gain in global diversity. And if we follow the Darwinian view that each species evolved only once in a given location, there is the biogeographical problem of attempting to explain the present irregular patterns of biodiversity. Aside from indirect causes, there is a fundamental question: in what part of the marine world did our present species arise? There is also the related question, how did these species arrive in their present locations? Although numerous correlations have been made between diversity and almost all aspects of the environment, it has become apparent that sea-surface temperature is the most important general control of geographical distribution.

The primary purpose of this investigation was to examine the evolutionary responses of continental shelf species to temperature and other immediate environmental effects that have resulted in increased diversity. The responses may be separated into two categories: (1) allopatric production of endemic species in provinces or regions due to barriers created by the global temperature gradient and other impediments, and (2) probable ecological or sympatric species production from the centres of origin and their essentially one-way longitudinal and latitudinal migrations outward to elevate the diversity of extensive areas.

Temperature gradient

The apparently close relationship between the global temperature gradient and the latitudinal gradient in species diversity has resulted in a general acceptance of cause and effect. There is a related theory which states that the sharp Cenozoic rise in marine species diversity was largely due to the packing of species into provinces, the provinces being primarily formed by the temperature gradient (Valentine, 1968; Jablonski et al., 2003). The first person to appreciate that temperature alone was a powerful controlling force was James Dwight Dana. As a young man, he took part in the United States Exploring Expedition (1838–42) and examined the distribution of corals and crustaceans. As a result, Dana (1853) was able to divide the surface waters of the world into several different zones based on temperature, and used isocrymes (lines of mean minimum temperature) to separate them. He made the prophetic observation that: ‘The cause which limits the distribution of species northward or southward from the equator is the cold of winter rather than the heat of summer or even the mean temperature of the year’. This observation proved to be valuable for both marine and terrestrial biogeography.

Three years later, Woodward (1856) examined the world distribution of the Mollusca and recognized 17 marine provinces, but did not discuss their temperature characteristics. He stated that, in order to be recognized as a province, at least 50% of the species should be peculiar (endemic). In the same year, Forbes (1856) delineated nine horizontal belts that extended across the Atlantic and Pacific oceans. Within each belt, he recognized one or more provinces and later (Forbes, 1859) noted that each province was an area where ‘.... there was a special manifestation of creative power’. In the late nineteenth and early twentieth centuries many publications described marine faunal regions, but without particular reference to temperature as a controlling factor.

Ekman (1935) completed the huge task of analysing all the pertinent literature on marine animal distribution, and published his results in a book written in German. In 1953, a second edition was printed in English (Ekman, 1953). He distinguished four major temperature zones: warm-water, warm-temperate, temperate (boreal or antiboreal), and arctic. Within the zones Ekman defined zoogeographical regions and sometimes subregions, but not provinces. He provided extensive information about the latitudinal distributions of many animal groups and about the phenomenon of bipolar distribution, but this was done with reference to temperature effects in only a few special localities.

In order to update Ekman's original work, I re-examined marine distributions and was able to benefit from the significant progress made by marine biologists during the previous 39-year interval (Briggs, 1974). On the basis of species distribution patterns available at that time, it was possible to identify discrete zoogeographical regions within each temperature zone and, within each region, one or more provinces could be distinguished. Although the individuality of provinces as subdivisions of larger regions had not been generally recognized, I regarded them as fundamental biogeographical entities. It was decided to designate an area as a province if at least 10% of its species were endemic. Although Woodward (1856) had advocated a threshold of 50% endemism for a province to be recognized, his provinces were much larger and species distributions were less well known in the mid-nineteenth century.

In the period between 1974 and the present day, most of the provinces have continued to be recognized, although some modifications were made as new data became available. The presence of such a large number of provinces prompts questions about their origin and significance. Forbes (1859) had stated that provinces, to be understood, must be traced back to their origin in past time. In the Mesozoic period, with its high sea levels, warm polar temperatures and lack of glaciation, the world existed in a greenhouse state (Fischer, 1984). In general, fossil distributions revealed a tropical Tethyan realm and a cooler Boreal or Temperate realm toward the poles (Hallam, 1994). The temperature of the high latitude waters of the Mesozoic was apparently equivalent to that of our present warm-temperate zones.

In the Triassic, the continents were joined together to form one continuous land mass called Pangaea. By the late Jurassic, Pangaea started to break apart and, by the end of the Cretaceous, most of the separations had taken place. By the late Cretaceous, the tectonic movements and the associated rise in sea level had produced an enormous increase in continental shelf habitat and stimulated a sharp rise in marine diversity (Clarke & Crame, 2003). Continental break-up also separated populations and initiated the formation of new biogeographical regions and provinces. But the end of the Cretaceous was marked by a drop in sea level, cooler temperatures and a mass extinction. Diversity dropped to about half its former level (Jablonski, 1989) and the recovery took c. 2 Myr (Erwin, 1998). By the late Palaeocene, marine temperatures along the shores of the Arctic Ocean had apparently declined into the cold-temperate range (Tripati et al., 2001).

By the time of the Palaeocene–Eocene boundary, c. 55 Ma, a global warming of 5–8 °C took place across a wide range of latitudes (Jenkyns, 2003). The apparent cause was the release of gas hydrates from continental margin sites. The warm period lasted until c. 49 Ma, after which the global temperature resumed its decline. The most profound cooling episode took place across the Eocene–Oligocene boundary c. 35 Ma (Hallam, 1994). Cold-temperate water around Antarctica descended to form the psychrosphere, the present cold bottom layer of the ocean. Two other warm periods took place during the Cenozoic, one c. 27–17 Ma, the other c. 5.3–3.5 Ma (Vermeij, 2004).

The temperature decline that followed the early Eocene warm period apparently resulted in the establishment of cold-temperate sea-surface conditions in the Arctic Ocean, North Pacific, North Atlantic, and the waters surrounding the Antarctic continent (Briggs, 2003). This resulted in a displacement of the warm-temperate waters into lower latitudes and a restriction of the tropics. By the late Oligocene, c. 25 Ma, the appearance of a major ice pack in the Antarctic (Bartek et al., 1992) indicated the presence of modern cold (−2 to +2 °C ) conditions. However, similar cold temperatures, now characteristic of the Arctic Region, were not established there until c. 2.7 Ma (Haug et al., 2005).

The penultimate result of the historic temperature decline which extended through most of the Cenozoic was the creation of a decreasing temperature gradient that led from the tropics to the poles. The ultimate result was the creation of the global organic diversity gradient. Despite the more than 30 theories for the formation of the latter (Turner & Hawkins, 2004), it seems likely that, if we knew the answer to the creation of the temperature gradient, then the mystery of the diversity gradient, or at least a large part of it, would be solved. Crame (2004) has pointed out that global cooling may have been promoted by four key tectonic events: (1) the isolation of Antarctica, (2) closure of the Tethys Sea to form the Mediterranean, (3) collision of Australia/New Guinea with Southeast Asia, and (4) uplift of the Central American Isthmus.

The foregoing tectonic events are related to continental closing, as opposed to the continental dispersal that took place in the Mesozoic. The Cenozoic realignment switched oceanic circulation from a predominantly equatorial to a strongly meridional trend (Crame, 2004). The circulation change enhanced the north–south gyrals in the Pacific and Atlantic oceans and led to the progressive development of biotic provinces on north–south shorelines. In addition, events (2)–(4) led to the imposition of east–west barriers in the tropical and warm-temperate regions. Over the course of the Cenozoic the number of biotic provinces increased from six to c. 43, the highest number in Phanerozoic history.

The packing of species and higher taxa into regions and provinces along gradients of latitude, longitude and depth has been suggested as an important cause of global diversity increase (Valentine, 1968; Jablonski et al., 2003). The idea of species packing comes from the evolutionary changes that take place within the bounds of each province. These changes produce endemic species and, depending on species density and other factors, a given province may export some of the species that it has produced. Although the packing of species into provinces, and the subsequent production of endemic species within those locations, probably accounted for a significant portion of the rise in Cenozoic diversity, the effects of certain special geographical areas need to be considered.

Centres of origin

It has been proposed that marine centres of origin have been functioning as evolutionary engines (Briggs, 2003). Four such centres have been recognized: the Antarctic, the North Pacific, the East Indies and the Southern Caribbean. Each centre has produced dominant, successful species that have spread over large geographical areas. More recently, Goldberg et al. (2005) have used the alternative term ‘macroevolutionary source’ for regions that have high rates of origination, and suggested the complementary term ‘macroevolutionary sink’ in reference to regions that obtain taxa through immigration. Their palaeontological contribution provided additional evidence that age distributions of extant taxa can be used to estimate rates of origination, dispersal and extinction. However, their substitution of an alternative term for centres of origin, a descriptive name that has been used since Darwin's time, appears to be less useful. Also, one may question their claim that there has been a ‘traditional assumption’ that centres of origin demonstrate high levels of endemism. In fact, it has been pointed out that within the tropics almost all reef areas that harbour relatively large numbers of endemics are located on the fringes, not within the centres of origin (Briggs, 2002).

The tropics

The centre of origin in the East Indies Triangle was completely established only c. 10 Ma, but its predecessor had existed in the Tethys Sea between Africa and Eurasia since the early Cretaceous. An Indo-Mediterranean Region within the early Cretaceous Tethys was recognized by Kauffman (1979) and, by c. 132 Ma, Eastern and Western Mediterranean subprovinces could be distinguished. By c. 124 Ma, a separate Caribbean Province was formed. The endemism that distinguished the latter was a reflection of the increasing distance between the New and Old World as the Atlantic Ocean became wider.

During the early Palaeogene (65–45 Ma), many extant families and genera evolved in the Indo-Mediterranean Region. They included the earliest coral reef fish assemblage consisting of eight families determined to be of Eocene age (Bellwood, 1996), with subsequent discoveries of parrotfishes (Streelman et al., 2002) and the family Triacanthidae (Santini & Tyler, 2003). The gastropod family Cypraeidae (Kay, 1990) and numerous bivalve and echinoderm higher taxa (Kafanov, 2001) were formed in that area. The climate grew colder beginning in the mid-Eocene, and Piccoli et al. (1987) were able to find fossil evidence of the displacement of molluscan taxa from the Indo-Mediterranean to the East Indies. The early Miocene collision between Africa and Eurasia eliminated the Tethys Sea and established the Mediterranean. The tropical biota trapped in the Mediterranean was gradually eliminated as the climate got colder.

In the meantime, the Tethyan fauna that had become isolated to form the Caribbean Province became divided into the West Central American and Antillean subprovinces (Kauffman, 1979). Some early contributions to the East Indies fauna may have been received from the Caribbean Province via trans-Pacific migration (Hallam, 1994). The late Cretaceous subdivision of the Caribbean Province may have been in response to the formation of a Central American archipelago. An early Central American isthmus may have also been formed at that time (Briggs, 1995), but its existence is still speculative. If there had been an isthmus, it disappeared in the Palaeocene, leaving a common American tropical fauna, until it was divided by the rise of the Panamanian Isthmus in the Pliocene.

It may be concluded that the modern, high-diversity biota of the Southern Caribbean was, in large part, derived from the Caribbean Province of the Tethys Sea, although some of it came from the Western Pacific across the East Pacific Barrier prior to the rise of the Panamanian Isthmus. The rich biota of the East Indies was inherited primarily from the Indo-Mediterranean Province via the Indian Ocean. In the northern part of the Western Atlantic, Pliocene–Pleistocene fluctuations in temperature resulted in many extinctions, but the Southern Caribbean was little affected and new species continued to originate (Allmon et al., 1996). From the time that the East Indies centre was well established in the late Miocene, and the Southern Caribbean centre in the Pliocene, dispersal of species from each centre began to augment the total diversity.

Considering the fact that the average life span of a marine species is c. 4 Myr (Sepkoski, 1998), and that the Pliocene began more than 5 Ma, this means that the origin and distribution of the great majority of our present species probably took place in the Pliocene and Pleistocene. Distributional patterns suggest that a large portion of the present species diversity originated in the two tropical centres. For example, with regard to the East Indies Triangle, the species diversity of reef fishes is likely to exceed 3000 (Briggs, 2005). Allen & Adrim (2003) estimated the number for the entire Indo-Pacific to be 3764. This means that more than three-quarters of the Indo-Pacific reef fishes, inhabiting a region that stretches more than two-thirds of the way around the world, are also present in the East Indies centre of origin. Also present are c. 450 species of hermatypic corals (Veron, 1995).

The concentration of species in the East Indies does not, in itself, prove that their formation took place in that area. However, several biogeographical patterns strongly point to the East Indies (Briggs, 1999): (1) a distance-correlated decrease in species diversity that extends outward from the East Indies, (2) an average outward increase in geological age, (3) historical dispersal tracks that radiate outward, (4) phylogenetic regression patterns indicating the peripheral locations of plesiomorphic species, (5) extinction patterns that originate in the East Indies and progress outward, and (6) indications from the mitochondrial DNA of some species that a decreasing gradient of genetic diversity extends outward.

Alternative explanations for the high diversity in the East Indies have been offered. These have usually involved theories dependent on: (1) an overlap of Indian Ocean and Western Pacific faunas, (2) a passive accumulation of species that had been formed elsewhere, and (3) historic movements of species via plate tectonics. The lack of evidence for these theories has been discussed (Briggs, 2004). More recently, the plate tectonic hypothesis involving island integration has been reiterated (Carpenter & Springer, 2005). But it is difficult to relate the present distribution of species, most of which are probably < 5 Myr old, to ancient tectonic movements. Bellwood et al. (2005) examined coral reef biodiversity in relation to energy, the mid-domain effect and reef area. Their best model incorporated area and the mid-domain effect, but did not include energy. However, it does not seem possible to apply the mid-domain effect when the longitudinal diversity peak on the equator lies far to the west of the midpoint of the Indo-Pacific (Mora et al., 2003). At a given time, one might expect to find a positive relationship between habitable area and species diversity, but this relationship can still exist and not affect the function of the East Indies as an evolutionary engine – the system is dynamic, so that origins are almost equalled by extinctions.

Mora et al. (2003) conducted a survey of coral reef fishes that extended all the way across the Indo-Pacific. They examined the longitudinal and latitudinal ranges of 1970 fish species, and found that on both axes the range midpoints clustered directly on the East Indies. Although the latitudinal peak was on the equator, the longitudinal peak was far to the west of the midpoint of the Indo-Pacific. This departure from a mid-domain effect indicated strong origination activity in the East Indies. Also, Mora et al. (2003) found 90 species that were endemic to the East Indies. These were apparently neo-endemics that had not begun to disperse outward. Their report concluded that the East Indies had played the major role in assembling communities throughout the Indian and Pacific oceans. Recent work on two invertebrate groups, cuttlefishes (Sepiidae) and cone shells (Conidae), also provides support for the East Indies centre of origin hypothesis (Neige, 2003; Vallejo, 2005).

Another interesting biogeographical pattern is morphological disparity. Within a given clade, it appears that high species diversity, as found in the East Indies, tends to be accompanied by a low level of morphological contrast among the species. Conversely, species located out on the horizontal periphery or in deep water often exhibit a greater variety in their structure, Why should this be so? Where speciation is most active, one might expect to find large numbers of closely related species. Over time, as species extend their range from their place of origin, extinction would take its toll leaving relatively few survivors. As a result, the remaining peripheral species often consist of plesiomorphic relicts that represent various evolutionary stages. Therefore a greater disparity might be expected. Examples of this pattern may be found in the strombid gastropods (Roy et al., 2001) and in the cuttlefishes (Neige, 2003).

The East Indies Triangle is the major centre of origin in the marine world because its influence, although predominant in the tropical Indo-West Pacific, extends to other tropical regions and to higher latitudes. Two principal barriers separate the Indo-West Pacific from the other tropical shelf regions. They are the deep-water East Pacific Barrier that lies between Polynesia and the New World, and the Old World Land Barrier comprising Africa and Eurasia. A variety of Indo-West Pacific species have crossed the former to become established in the Eastern Pacific. These include 80 fishes (Robertson et al., 2004) and 61 gastropod molluscs (Emerson, 1991). Conversely, there have been few successful migrations in the opposite direction. Twenty-two shore fishes have apparently migrated westward, but 12 of them do not extend past Hawaii. None of the molluscan lineages in the Eastern Pacific has been able to invade westward (Vermeij, 2004).

About 95% of the Eastern Pacific coral species are recent immigrants from the Indo-West Pacific (Robertson et al., 2004). This predominantly eastward invasion has occurred despite the fact that the north equatorial current has been shown to carry larval stages from the Eastern Pacific towards the Indo-West Pacific (Scheltema, 1988). Similarly, the other boundaries of the Indo-West Pacific appear to function essentially as one-way filters. Twenty-one gastropod species and a similar number of fishes from the Indo-West Pacific have been able to round the Cape of Good Hope to colonize the tropical Atlantic, but there seems to have been no successful migration in the opposite direction (Vermeij, 2004). Since the opening of the Suez Canal in 1869, more than 200 species of Indo-West Pacific organisms have established themselves in the Mediterranean, but only about a dozen have taken the reverse course (Galil, 1994). When the biota of the other three tropical regions (Eastern Pacific, Western Atlantic, Eastern Atlantic) is examined, the relationship to the Indo-West Pacific seems obvious. Most of the families and a large fraction of the genera are shared among all four.

Although the rise of the Isthmus of Panama did not form a complete marine barrier until the late Pliocene, there are indications that the reef fauna of the Caribbean began to separate from that of the Eastern Pacific in the late Miocene, c. 7 Ma (Muss et al., 2001). During the intervening time a new evolutionary relationship became established within the Atlantic. A diversity centre developed within the southern part of the Caribbean Sea, but its species richness is far less than that of the East Indies. For example, the latter probably supports more than 3000 fish species compared with c. 700 in the Caribbean (Rocha, 2003). Similarly, there are c. 450 hermatypic coral species compared with c. 50 in the Caribbean (Veron, 1995).

The shelf fauna of the Eastern Atlantic tropics is separated from that of the Caribbean by the deep-water Mid-Atlantic Barrier. The overall species diversity of the Eastern Atlantic is only about one-third that of the Caribbean (Briggs, 1985). Recent research (Joyeux et al., 2003) has revealed the presence of 92 trans-Atlantic species of reef fishes, the great majority belonging to well developed Caribbean genera. Circumstantial evidence indicates an eastward migration, with only four species apparently having travelled in the opposite direction. Within the Western Atlantic, Southern Caribbean species have apparently been penetrating northward into Florida and Bermuda and southward into Brazilian waters (Rocha, 2003). During the past 2 Myr, the Eastern Atlantic has received at least 41 molluscan species from the Western Atlantic, and c. 14 migrated in the opposite direction (Vermeij, 2004). These predominantly outward migrations are indications that the Southern Caribbean has been operating as a centre of origin.

In addition to the enormous diversity of species that exist in the shallow waters of the tropics, there is good evidence that, over time, tropical species have been successful in invading deeper waters and the temperate waters of higher latitudes. Jablonski et al. (1983) drew attention to onshore–offshore patterns in the evolution of Phanerozoic shelf communities. In more recent years, several palaeontologists provided additional evidence of onshore-to-offshore replacements, and discovered that, in general, new species, genera and families had evolved under high-diversity conditions. This led to the common observation that ‘diversity begets diversity’.

Over time, the onshore-to-offshore replacement sequence has had a cumulative effect in the deep sea. Although the cold-water centres in the North Pacific and Antarctic have made significant contributions to the slope and abyssal faunas, so have the tropics. There are many families of deep-sea animals that live only at low latitudes, so the faunistic centres in the Pacific and Atlantic may be contributing directly to the deep sea (Zezina, 1997). On the other hand, there is no evidence of any deep sea clade being able to establish itself in shallow, tropical waters (Vermeij, 2004).

With regard to the relationship of the shallow-water tropical and temperate biotas, it has been noted that the warm-temperate zone that borders the tropics to the north and south, possesses genera and families that are mostly of tropical affiliation. It has also been discovered that the historical movements of species between the tropics and temperate waters have apparently been entirely one way. In a survey of molluscs and barnacles that originated from 20 to 25 Ma, Vermeij (2004) found that 29 American and nine Asian clades in warm-temperate to tropical waters had given rise to cold-adapted species, but no temperate clades had spawned tropical species. Crame (2000) concluded that the steep latitudinal gradients of the youngest bivalve clades provided additional information on dispersal, and that the tropics could be seen as a species pool supplying bivalve taxa to high-latitude and polar regions.

As can be noted from the family history of marine diversity (Clarke & Crame, 2003), a significant increase began with the continental break-up in the early Jurassic, but the steepest rise started in the early Cenozoic. The Cenozoic increase was especially marked at the lower taxonomic levels, with species diversity rising perhaps an order of magnitude (Crame, 2004). There were significant radiations of neogastropods, heteroconch bivalves, cheilostome bryozoans, decapod crustaceans and teleost fishes. Considering that these comparatively young groups show strong latitudinal diversity gradients, it can be inferred that their major radiation events were centred in the tropics.

Within the Indo-West Pacific, it is apparent that the centre of diversity and of evolutionary innovation lies within the bounds of the East Indies Triangle. This concentration of power is exemplified by the recent study of the ranges of fish species across the Indo-Pacific (Mora et al., 2003) where, on average, 86% of the species found in the outlying areas were also present in the Triangle. If, as the fossil data indicate, diversity does beget diversity at species, family and generic levels, then the East Indies centre may be the place of origin of most of the young lineages that have successfully penetrated the cooler waters of higher latitudes and greater depths. The Southern Caribbean, the secondary tropical centre of origin, could also have been effective in this manner.

A considerable amount of tropical species diversity is due to the evolution of herbivory, a feeding habit that has become widespread in the tropics but remains relatively rare in temperate waters. It has been noted (Vermeij, 2004) that herbivore-containing clades exist within the molluscs, annelids, arthropods, echinoderms and vertebrates. Furthermore, the herbivore taxa occupy the more derived positions within their respective evolutionary trees, and most are unknown prior to the Cenozoic. Herbivory is found within 10 clades of bony fishes that occur mainly in the tropics. Most of the herbivorous clades in the Indo-West Pacific are represented by more species in the East Indies centre than anywhere else.

Investigations of fish diets have revealed that tropical reef fishes show an evolutionary trend towards taking advantage of relatively low-energy food resources such as algae, sea grasses, sponges, detritus and cnidarians (Harmelin-Vivien, 2002; Floeter et al., 2004). In some locations as many as 57–79% of species were dependent on such resources, especially algae and sea grasses. This suggests that a considerable portion of the tropical marine diversity may be attributed to the presence of species that have evolved, by means of ecological specialization, to utilize low-energy food resources. This shift to an alternative food supply under highly competitive conditions suggests that sympatric speciation may have been involved. It appears that, when such tropical lineages attempt to invade cooler waters, the increased energy demand constitutes a difficult physiological barrier. Some clades manage to exist at higher latitudes by becoming omnivorous or by a seasonal switching between herbivory and carnivory.

Temperate and polar centres

In the cold and cold-temperate zones, the other two centres of origin have also been effective in adding to Cenozoic diversity. Of the two, the North Pacific centre has been the most broadly influential. It was formed c. 40 Ma but did not achieve its present influence until the opening of the Bering Strait permitted the Great Trans-Arctic Biotic Interchange. The invasion into the Arctic-North Atlantic produced enormous ecosystem changes. Some of the migrations may have begun as early as 12 Ma, but apparently most took place c. 3.5 Ma, before the Arctic Ocean was ice-covered and when the temperature was still in the cold-temperate range. New information regarding molluscan species in the North Atlantic (Vermeij, 2004) indicates that at least 143 invading species colonized European shores, while 176 settled in eastern North America. At most, 24 species invaded the North Pacific from the Atlantic. On the eastern American rocky shores, the invaders now comprise the majority of common species.

The North Pacific has contributed a variety of organisms to the cold-temperate southern hemisphere and even to the Antarctic. The migrations took place primarily via isothermic submergence, whereby the species concerned could maintain a suitable temperature by moving beneath the tropics at great depth. For example, two fish families of North Pacific origin are represented by numerous species around the Antarctic continent. There are 90 species belonging to the families Zoarcidae and Liparididae, together comprising > 40% of the Antarctic fish fauna. Many other clades of North Pacific origin have reached the Southern Ocean, but most did not penetrate as far south as the Antarctic.

The external influence of the Antarctic Region, with respect to the surface waters, has generally been limited. Many species produced in the region have managed to migrate to the surrounding cold-temperate waters of the Sub-Antarctic. A few species, such as some penguins, fishes and molluscs, have extended their range much farther. The greatest external influence has been in the deep sea. A variety of deep benthic organisms were apparently introduced to that habitat via thermohaline currents originating around Antarctica.

Speciation

In inquiring about the origin of contemporary marine species diversity, one needs to take into consideration the evident difference in modes of speciation between the centres of origin and other areas. Recent studies combining the phylogeny and ecology of natural populations have emphasized the role of ecological factors in speciation (Via, 2002). Studies of parallel speciation have provided a strong case for sympatric speciation and for natural selection in generating reproductive barriers (Johannesson, 2001). Briggs (2005) proposed that, within the East Indies, the high species diversity, the production of dominant species, and the presence of newly formed species are due to natural selection being involved in reproductive isolation, the first step in the sympatric speciation process.

The Darwinian view maintains that natural selection directly favours the multiplication of species during ecologically based sympatric speciation (Coyne & Orr, 2004). Under this view, allopatric species are accidental by-products of genetic divergence. In other words, when a physical barrier separates a formerly continuous population, natural selection is not involved in the process of reproductive isolation. If natural selection usually produces better adapted species, then those produced by allopatry are at a disadvantage. Furthermore, species formed by sympatry usually evolve much more quickly. In sympatric Drosophila populations, speciation is completed in c. 200,000 years, but allopatric populations require c. 2.7 Myr (Coyne & Orr, 2004).

The East Indies example does not mean that sympatric speciation is confined to centres of origin. This mode was suggested by the presence of sympatric sibling species in many locations (Knowlton, 1993), and has now been proven in several places (Hellberg & Vaquier, 1999; Hendry et al., 2000; Dawson et al., 2002; Jones et al., 2003) and strongly suggested in others (Munday et al., 2005; Rocha et al., 2005). Sympatric speciation usually takes place when there is opportunity for the occupation of additional habitat or when there is an alternative food supply available. The same ecological opportunities apply to parapatric speciation. Species flocks resulting from rapid bursts of cladogenesis are well known among freshwater fishes, but have been investigated only recently in various marine clades. By using molecular phylogenies to study variation in diversification rates among lineages, Ruber & Zardoya (2005) were able to find elevated rates of cladogenesis in six different groups of marine fishes. Explosive radiation leading to the formation of a species flock has been found in a marine gastropod genus (Duda & Rolan, 2005). Sexual selection under sympatric conditions has contributed to rapid speciation in freshwater fishes (Salzburger & Meyer, 2004), and should be anticipated in marine clades.

There is a difficulty with terminology that arises in descriptions of the speciation process. While allopatry, whether caused by dispersal or vicariance, is clearly understood, various terms have been employed when speciation occurs within a continuous population. The designations parapatric, sympatric, competitive and ecological are all being used currently to describe speciation events that occur without initial physical separation. But all four terms essentially define the same process: the achievement of reproductive isolation by means of selection for an alternative environment or food source. And speciation that is initiated by natural selection is fundamentally different from that initiated by allopatry. Although one result of such a sympatric type of speciation may be the formation of adjacent or parallel species, often called parapatric, their origination does not appear to differ from that of other non-allopatric species.

As most species now isolated in regions and provinces by physical barriers (temperature, distance, currents) were probably formed by allopatry, they would be relatively slow in producing endemics. Therefore the species-packing process would be comparatively slow. Its effectiveness on the general level of species diversity could theoretically be calculated by adding together the numbers of all the endemic species that exist in all the provinces – unfortunately an impossible task at the present state of our knowledge.

Conclusions

From a global viewpoint, it appears that plate tectonics can account for the steep rise in diversity that began with the onset of the Jurassic Period c. 200 Ma. This time marked the beginning of the break-up of Pangaea, which meant a rise in sea level, the formation of biogeographical barriers, an increase in continental shelf area, and an increase in global temperature. All four are important factors in the stimulation of marine diversity. As the continents moved farther apart through the course of the Jurassic and Cretaceous, the barrier effects became accentuated while the sea level and temperature remained high, hence the increase in diversity continued until the end of the Cretaceous.

At the time of the Cretaceous/Tertiary boundary, the sea level fell, the temperature dropped, and a mass extinction took place that dramatically lowered marine diversity to about half its former level. The recovery of diversity took c. 2 Myr. Although considerable temperature fluctuation took place during the course of the Cenozoic, there was a general cooling trend. The result was the establishment of the present tropics-to-poles temperature gradient and the consequent species (and generic and family) gradient. The first proximal cause for the rise of Cenozoic diversity was the formation of biogeographical regions and provinces due to the temperature gradient, promoted by tectonic movements and the modification of oceanic currents.

The second proximal cause for the continued diversity trend was the establishment of the present centres of evolutionary origin. An old tropical centre was located in the Tethys Sea of the Mesozoic. In the Triassic, when there was an absence of strong latitudinal gradients, it may have been the source of most speciation events. Barrier effects came into play with the advent of continental break-up in the remaining two periods of the Mesozoic. In the Palaeogene of the Cenozoic, the Tethys centre, located in the Indo-Mediterranean Province, was the focus of important evolutionary innovations including the origin of extant families and long-lived genera. At the species level, which includes most of the origins of the past 5 Myr, all four of the currently recognized centres of origin became important.

Does the large number of species produced from the centres, and subsequently spread over extensive parts of the world, exceed the total produced within all other regions and provinces? The majority of species now isolated in regions and provinces by physical barriers (temperature, distance, currents) were probably created by allopatry, so their formation has been relatively slow. Therefore the species-packing process would also have been slow. The ecological or sympatric (or parapatric) process in the centres of origin, which proceeds via natural selection, apparently produces better-adapted species, and does so at a rate that is perhaps 20 times faster than the allopatric process, suggesting that the exponential rise in diversity during the Cenozoic may be primarily due to production from the centres of origin. An important evolutionary development in the tropical centres was an enormous Cenozoic multiplication of species that took advantage of low-energy food sources. Such species now comprise a large portion of the diversity on the continental shelves of the tropics. Considering that the formation of the ‘low-energy’ species took place in the tropics under high-diversity conditions, and that they had shifted to alternative food sources, it seems probable that many of them must have speciated via the sympatric process.

In terms of total species diversity it is obvious that, once a successful species extends its range far away from its place of origin, it will be subjected to a variety of barriers that will interrupt its genetic integrity. Over time, the barrier effects may result in allopatric speciation and ultimately the generation of several related species from one ancestral population. If the production of each successful species by sympatry in a centre is followed by several more in peripheral allopatry, then most of our present species must have been produced by the latter process. But, of the species produced in the centres of origin, we do not know how many actually give rise to descendent species. Also, there is the problem of secondary allopatry whereby formation of a barrier will result in daughter species from an originally allopatric parent. At this time, we cannot provide a dependable estimate about the number of marine species that owe their origin to allopatry vs. sympatry. However, it is possible to emphasize that, aside from the rare occurrence of polyploidy, there appear to be only two fundamental kinds of speciation in the marine environment: allopatry, which does not involve natural selection to achieve reproductive isolation; and sympatry (in the broad sense), which does depend on natural selection.

Although this work is devoted mainly to the immediate causes of species diversity and the theoretical geography of the speciation processes, it is important to keep in mind that all species are not born equal: those produced under the highly competitive conditions found in the centres of origin are the ones most likely to spread out and produce continuing lineages. The four centres of origin are the primary sources of evolutionary power and innovation in the marine world. The species that they produce contribute to evolutionary change by gaining new territory and, in so doing, often cause the loss of territory by species that are less well adapted.

Acknowledgements

I wish to thank Eila Hanni and Brian Bowen for their assistance with the manuscript.

Biosketch

John C. Briggs was named Professor Emeritus on his retirement from the University of South Florida in 1990. His research deals primarily with the origin and distribution of contemporary groups of organisms. His biogeographical books include Marine zoogeography (McGraw-Hill, 1974), Biogeography and plate tectonics (Elsevier, 1987), and Global biogeography (Elsevier, 1995). In 2005 Professor Briggs received the Alfred Russel Wallace Award from the International Biogeography Society for his lifetime contributions to biogeography.

Editor: David Bellwood

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