Despite differing geological and evolutionary histories between the Indo-Pacific and Atlantic biogeographical realms, our results show limited variation in the ages of their constituent coral reef fish faunas. The CIP and its peripheral regions have all experienced recent divergence events, with no detectable difference in the mean ages of reef fish species among regions in the Indo-Pacific. Atlantic regions have also experienced recent divergence events, with mean ages similar to those of the Indo-Pacific. Furthermore, ages of endemic species do not differ from more widespread species. Therefore, our results do not support the indiscriminate use of endemic species as markers of species origination. Interesting patterns of diversification in isolated locations provide insights into the processes underlying endemism and peripheral speciation. Specifically, we report notable differences between the Red Sea and the Hawaiian Islands in the timing of divergence events and in patterns of contemporary geographical distribution of endemic species.
The Indo-Pacific and Atlantic realms are undoubtedly characterized by unique assemblages of coral reef fishes (Briggs & Bowen, 2012; Kulbicki et al., 2013). While some species have attained circumtropical distributions, most species are restricted to a particular realm and share the influence of its historical periods of isolation (Kulbicki et al., 2013). Vicariance events such as the closure of the Tethys seaway (Steininger & Rögl, 1984) and the rise of the Isthmus of Panama (Coates & Obando, 1996) have produced diffuse signals of vicariance among reef fish lineages, while soft hydrological barriers to dispersal can result in tightly concordant vicariance (Cowman & Bellwood, 2013b). Furthermore, each region has a markedly different amount of space for reef fishes to occupy, which has varied through time and may have influenced the rate of species divergence or extinction (Bellwood & Wainwright, 2002; Renema et al., 2008). Despite the potential for temporally diffuse or concentrated vicariance events, and variable habitable area within each realm, we found few significant differences among the ages of constituent species using two approaches for age comparison. On average, recent divergence of extant species has occurred throughout the past 1–5 Myr in the Indo-Pacific and Atlantic realms, suggesting similar timing in the divergence of reef fishes, despite different geological histories and different contemporary patterns of biodiversity.
Differences between the two approaches in the ages of widespread species in the Indo-Pacific realm suggest that extinction may have resulted in substantial overestimation of species' ages using the full-phylogeny approach, whereas the larger magnitude of change in mean species age in the WA region, relative to other regions, suggests that extinction may have had the greatest influence on the ages of extant species in this region. The Atlantic has experienced a substantial loss of marine taxa during a period of faunal turnover in the Plio-Pleistocene (Bellwood, 1997; O'Dea et al., 2007), which may explain the differences we observed when comparing full-phylogeny and sister-species approaches.
In the Atlantic, widespread species are younger than their region-restricted counterparts. However, we found just two species with distributions spanning the Eastern and Western Atlantic regions. The low number of widespread species in the Atlantic may be due in part to the relatively low overall coral reef fish biodiversity of this realm (Bellwood, 1997; Kulbicki et al., 2013), but it may also indicate that regional spatial structure is an important characteristic of Atlantic species (Bender et al., 2013). In comparison to the Indo-Pacific, the Atlantic has fewer centrally located islands available to facilitate range expansion, which may produce more defined spatial structure among its faunal constituents.
We detected more variation in the ages of reef fishes between regions than among realms, with younger ages in the CIP than in the WI and CP. Younger ages of reef fish species in the CIP, although not significantly different from random permutations, lends some support to the centre of origin or centre of survival hypotheses. Recent models of coral reef fish evolution and dispersal over the last 65 Myr demonstrate that the IAA (located within the greater CIP region) has played a number of different roles, supporting the accumulation, survival, origination and export of species (Cowman & Bellwood, 2013a). More specifically, models suggest that since the Miocene (23 Ma) the IAA has been characterized by exceptionally high rates of species origination (Cowman & Bellwood, 2013a). This may explain the slightly younger species' ages we obtained for the CIP relative to adjacent regions that, according to the models, were colonized by lineages that originated in the IAA during this time (Cowman & Bellwood, 2013a).
If vicariance has played a major role in recent species diversification, it would have a neutralizing effect on any potential patterns between vicariant regions when comparing species' ages using the full-phylogeny approach. For example, the rise of the Isthmus of Panama produced geminate species pairs with a shared age that are now distributed either side of the barrier. Therefore, when comparing the ages of species from the WA and the ETP, the ages of geminate species pairs are considered for both regions and neutralize any differences in age structure between them. However, patterns of relative age between realms and regions remained constant, with the exception of species in the WA region, when we accounted for such covariance of ages using the sister-species approach.
Our methods considered only extant species and their lineages, and therefore were not capable of resolving historical evolutionary differences that may have distinguished biogeographical areas. The protocols we applied to maximize sampling of extant species meant that generic sampling achieved within families was limited and we were not able to resolve deeper splits in the phylogeny with confidence, precluding an assessment of historical differences among lineages. Instead, we have focused on recent speciation events because it is unlikely that many older species have survived to the present day. If older species have survived and also given rise to other species through time (i.e. peripheral budding sensu Hodge et al., 2012), their true age may be masked by recent speciation events. Thus, historical signals are largely overwhelmed by recent speciation. Different geological and evolutionary histories among regions have probably shaped lineages, but speciation has largely been shaped by events in the past 1–5 Myr.
Endemic species in the Red Sea and Hawaii displayed different age distributions when compared with each other and with the underlying age distribution of the full phylogeny, suggesting that distinctive processes of diversification have operated at these peripherally isolated locations. Our topological and chronological hypotheses of Red Sea and Hawaiian endemic species agree with previous phylogenetic hypotheses for Chaetodon (Fessler & Westneat, 2007; Bellwood et al., 2010; Craig et al., 2010), Anampses (Hodge et al., 2012), Chlorurus (Choat et al., 2012), Larabicus (Westneat & Alfaro, 2005; Cowman et al., 2009; Kazancıoğlu et al., 2009), Scarus (Choat et al., 2012) and Thalassoma (Bernardi et al., 2004), offering additional confidence in the chronogram.
Red Sea endemics appear to have arisen steadily throughout the last 16 Myr, roughly 10 Myr after the sea first appeared (Bosworth et al., 2005). They include the oldest extant lineage in the WI region, Larabicus quadrilineatus, which is estimated to have diverged 14.7 Ma, around the time when the Red Sea was becoming increasingly isolated from the Mediterranean (Bosworth et al., 2005) and the Arabian hotspot was dwindling (Renema et al., 2008). In the recent geological past, the Red Sea has experienced volatile changes in temperature and salinity (Biton et al., 2008). The effects of these environmental fluctuations have reportedly caused mass extirpation of marine organisms including planktonic foraminifera (Hemleben et al., 1996). Our results, as well as other phylogeographical studies of reef fishes (DiBattista et al., 2013), suggest that the Red Sea, or the adjacent Gulf of Aden, has sustained coral reef fish lineages (and presumably coral reefs) throughout these environmental fluctuations. Older endemic lineages, such as L. quadrilineatus, are likely to have survived outside of the Red Sea during extreme environmental periods and subsequently re-invaded when the Red Sea opened up to the WI region c. 5 Ma and the environment became suitable for the maintenance of coral reefs (Siddall et al., 2003; Bosworth et al., 2005). The majority of Red Sea endemics (75% of those studied herein) diverged after this time. The continuity of the continental shelf to the east and south of the Red Sea, in combination with its relative close proximity to the IAA, is likely to have facilitated the ongoing divergence of lineages throughout the last 16 Myr.
In contrast to the Red Sea, the Hawaiian Archipelago is located in the central Pacific Ocean and is part of the larger Hawaiian–Emperor seamount chain, a series of volcanic islands and atolls separated by oceanic channels. Our data suggest that colonization of the Hawaiian Islands has occurred independently for multiple species belonging to the genera Chaetodon, Anampses and Thalassoma. This is consistent with previous phylogenetic hypotheses (Bernardi et al., 2004; Fessler & Westneat, 2007; Craig et al., 2010; Hodge et al., 2012). Multiple models of diversification have probably led to the divergence of Hawaiian endemics including, but not limited to, successive colonization/division and peripheral budding (sensu Hodge et al., 2012). For example, Craig et al. (2010) proposed that a closely related Chaetodon species complex containing C. punctatofasciatus, C. pelewensis and C. multicinctus, originated in the western Pacific, spread through the South Pacific Islands and finally colonized the Hawaiian Islands. With our inclusion of the closely related WI species, C. guttatissimus, we find that the diversification of species in this clade could fit a successive division or colonization model, with initial separation between the Indian Ocean and the CIP/CP, followed by separation between the CIP/CP and the Hawaiian Islands. However, the region of origination of this lineage remains unclear.
In contrast to the ongoing cladogenesis in the Red Sea, we found evidence for two distinct waves of divergence among Hawaiian endemics. The two waves of divergence (0–3 Ma and 8–12 Ma) occurred either side of a broad period of increased primary productivity (Dickens & Owen, 1999) that coincided with increased cladogenesis for a wide range of taxa in the Indo-Pacific, including reef fishes, between 3.5 and 9.0 Ma (Renema et al., 2008; Reid et al., 2010; Cowman & Bellwood, 2013a,b). The first wave coincides with the late Miocene–Pliocene (9–12 Ma) when deep-water circulation reorganization occurred as a result of the reduction in deep-water exchange between the Atlantic and Pacific Oceans through the Panamanian gateway prior to the emergence of the isthmus (Lyle et al., 1995). These changes in deep-water circulation caused disruption to large-scale ocean circulation patterns (Butzin et al., 2011). Further evidence suggests that atmospheric and oceanic circulation intensified about 10 Ma (Rea & Bloomstine, 1986) and during the glacial periods of the past 1.2 Myr (Hall et al., 2001). These changes in ocean circulation and intensity may have produced more favourable conditions for founder populations of reef fishes to reach the Hawaiian Islands and establish themselves, ultimately leading to the divergence of peripatric populations and the formation of endemic species.
Different proportions of allopatric and sympatric sister-species among Red Sea and Hawaiian endemics provides additional support for the operation of distinctive processes of diversification at these peripherally isolated locations. Red Sea endemics have equal proportions of allopatrically and sympatrically distributed sister-species, and approximately one-third appeared as sister to a clade. Secondary endemism, where a primary endemic gives rise to one or more subsequent endemics (Rotondo et al., 1981), appears likely to have operated in the Red Sea province given the sympatric distribution of the well-supported sister-species pair: Scarus persicus and Scarus ferrugineus, both Red Sea/Persian Gulf endemics (Choat et al., 2012). Our results, in combination with knowledge of the dynamic geological and environmental past of the Red Sea, suggest that a number of speciation modes may have operated through time and that both allopatric and sympatric speciation are likely to have played a role in generating Red Sea endemics.
While a number of speciation modes may also have led to the diversification of Hawaiian endemics, our results reveal potential key differences between the two isolated provinces. As in the Red Sea, one-third of Hawaiian endemic species are sister to a clade. However, allopatric distributions constitute the bulk (78%) of endemic species' distributions in the Hawaiian Islands. With such a low level of sympatry it seems unlikely that either sympatric speciation or secondary endemism has been important in the evolution of Hawaiian endemic reef fishes. Rather, allopatric speciation, probably in the form of peripatric speciation, appears to have been the dominant mode in generating Hawaiian reef fish endemics. The topological relationships and estimated ages of sympatric endemic species (between 8 and 12 Ma), combined with the low levels of average overlap (< 10%), suggest that peripheral budding (sensu Hodge et al., 2012) may be a key model under which Hawaiian endemic reef fishes have diverged.