CAPITULO 2 MARCO TEORICO
2.7 El Elemento Torio
This study represents the most comprehensive phylogenetic and phylogeographic treatment of the family Platycephalidae given the geographical scale and the number of species analysed. The results provide novel insights into the evolutionary relationships in the group that challenge a number of previous hypotheses proposed for this family. However, these findings agree with the subfamily split suggested by Imamura (1996) and confirm a number of intra-generic relationships proposed by Imamura (1996) and Keenan (1988, 1991).
4.5.1 Latitudinal diversity gradients in temperate & tropic regions
The increased species richness from the poles to the tropics represents one of the most pervasive biodiversity patterns (Allen & Gillooly 2006; Hillebrand 2004; Kraft et al.
2011; Smith et al. 2012; Willig et al. 2003). However, a number of cases where taxonomic groups display a converse relationship to the conventional LDG have been reported (reviewed in Kindlmann et al. 2007; Rivadeneira et al. 2011).
The main division of flathead subfamilies, the Platycephalinae and Onigociinae, suggests early and long-term isolation of these two groups followed by distinct genealogical trajectories. Diversification patterns observed across the Platycephalinae, together with the greater species diversity in higher latitudes (Figure 4.3), is suggestive of a temperate origin followed by species expansion towards the tropics. This observation is not supportive of the ‘out of the tropics’ hypothesis (Jablonski et al. 2006), and is more indicative of an inverse, ‘out of the deep south’ origin (Rivadeneira et al. 2011). Furthermore, as taxa confined to southern Australia are genealogically older compared to their tropical relatives (Figures 4.3- 4.5), an age versus latitude assumption appears to have no bearing on diversity patterns (i.e. groups originating in the tropics are expected to be older with higher latitude taxa nested within lower latitude taxa).
Conversely, onigociins appear to have maintained a tropical distribution throughout their evolutionary history. Furthermore, the higher accumulated species diversity in this subfamily is presumably at least partly due to their existence in tropical regions for longer periods of time (the subfamily has ~three-fold more extant species than the Platycephalinae based on current taxonomy). However, this trend is not related to the longer history of the tropics per se (i.e. the “age of the tropics” hypothesis) as the early diversification of ancestral lineages, contributing to the current diversity in both the Onigociinae and Platycephalinae, is associated with similar geological periods (30 to 20 Ma).
4.5.2 Diversification in the tropics
A variety of ecological and evolutionary factors altering diversification rates and survival optima across latitudes can account for LDGs (Floeter et al. 2004; Lappalainen & Soininen 2006; Mittelbach et al. 2007; Roy et al. 2000; Smith et al. 2012; Wiens & Donoghue 2004). Faster extinction rates at high latitudes might be expected due to greater environmental variability, both seasonally and over longer timescales (Dynesius & Jansson 2000). However, disentangling these rates from low diversification rates, processes that can produce the same clade size (Ricklefs 2007), is challenging in the absence of palaeontological data.
The phylogeographic patterns observed across flathead lineages at both low and high latitudes correlate well with climate-driven processes and associated exposure to vicariant barriers. The majority of flathead species occupy relatively homogenous sand or muddy coastal environments and coastline length positively correlates to coastal diversity (Tittensor
et al. 2010). Given that the tropical belt (20o N to 20o S) represents the largest eco-climatic
zone globally (Gaston 2000), under favourable environmental conditions, dispersal across this region not only offers opportunities for expanding the ranges of species, but also increases their access to additional refugia during glacial coastline contractions. The periodic exposure of the Sunda Arc and the Torres Strait land bridges represent some of the most conspicuous examples of vicariant barriers splitting lineages and clearly play a crucial role in species diversification across the region (Carpenter et al. 2011; Mirams et al. 2011).
Higher diversification rates in the tropics may also relate to increased evolutionary speed. It has been suggested that increased temperature and/or metabolic rates may be driving faster speciation rates in tropical regions (Allen & Gillooly 2006; Fuhrman et al. 2008). However, LDGs have been observed in terrestrial endotherms (e.g. mammals and birds) suggesting the influence of temperature is not sufficient to explain latitudinal trends in species diversity (Mittelbach et al. 2007). This conclusion may not be applicable to the marine environment as warm-blooded marine mammals have greater species diversity at higher latitudes (Tittensor et al. 2010). Additionally, see Gillman et al., (2009) and Weir & Schluter (2011) for discussion on the potential of increased mutation rates for mammals in warmer environments.
4.5.3 Migration direction since the Eocene
Fossil otoliths of flatheads are first reported in the Palaeo-Mediterranean from the late Eocene along with many other extant IWP endemics (Girone & Nolf 2009). Many of these lineages, once common to Western Europe during the Eocene, are now confined to refugia in
temperate Australian and New Zealand waters (Vermeij 1986). It is unclear whether these groups were already widespread at the time or subsequently migrated (en masse) to these southern waters. The uninterrupted access to the ancient Tethys Sea (Rögl 1999) and tropical global climate (~20oC at high latitudes Liu et al. 2009) for most of the Eocene suggests that favourable conditions existed for lineage dispersal between low and high latitudes. Ancestral flathead lineages, present on the Australian continent during the Eocene, would have been exposed to the dramatic shift in climate during the Eocene-Oligocene boundary (~5oC drop in ocean temperatures at high latitudes; Liu et al. 2009). This temperature shift may have provided the evolutionary impetus for their isolation and early success in temperate waters as lineages that did not adapt to this rapid shift either retreated from high latitudes to tropical climes or became extinct (Prothero 1994).
The Oligocene climatic shift was also responsible for the formation of the cold psychrospheric deep waters (100–700 m depths, ~10oC; McKenzie 1991) and may have triggered formation and diversification within the two sub-families. Imamura’s (1996) hypothesis suggests the platycephalids may have evolved in deep-water environments, in the same way ancestral Bembridae and Parabembridae families (Figure 4.1) likely occupied the continental slope. In addition, basal lineages within the Platycephalidae, such as Ratabulus
and the P. aurimaculatus, P. conatus and P. richardsoni group,appear to reflect deep-water origins (Figure 4.6b). Early flathead fossils are among fish assemblages that include both shallow and deep-water lineages (Girone & Nolf 2009; Long 1982) offering no definitive clarification.
Collision between the Australian and Eurasian Plates from the early Miocene (~23 Ma) likely favoured colonisation and subsequent diversification of tropical IWP platycephalin lineages (Figure 4.4) due to the formation of extensive, shallow-water environments providing corridors for dispersal (Hall 2009). In contrast, phylogeographic patterns evident in the Onigociinae suggest the group mainly retreated to the tropics, prompted by the Eocene climatic shift; exceptions being isolated lineages (e.g. L. inops and T. cirronasa) that adapted and persisted in temperate conditions of southern Australia. Alternatively, these onigociin lineages may have subsequently migrated to southern Australia in the early Miocene. The latter hypothesis finds support in the molecular clock approximations (Figure 4.5). Tropical species repeatedly invaded the southern fauna through the early-Miocene climatic optimum (O'Hara & Poore 2000; Wilson & Allen 1987). The sudden mid-Miocene glaciation, responsible for a ~7oC drop off the South Tasman Rise (Zachos et al. 2001), coincided with
the disappearance of flatheads and other Indo-Pacific endemics at high latitudes across northern Europe and the Palaeo-Mediterranean (Steurbaut 1984) and may have been responsible for the depauperate onigociin lineages that persist in temperate Australia.
The earliest evidence of flatheads occupying southern Australia is a mid-Miocene fossil from Victoria (Long 1982). If we assume migration of a platycephalin group into southern Australia during the early Miocene climatic optimum, then we might expect tropical taxa to represent the most ancestral lineages. Given their current distributions and their molecular clock approximations, an earlier flathead presence in Australia is plausible (i.e. presence there prior to the Eocene-Oligocene climate shift) followed by subsequent movement and adaptation of derived lineages to warmer, tropical waters through the early to mid-Miocene climatic optimum.
4.5.4 Diversification in the mid-Miocene
High levels of diversification are observed in ancestral, temperate platycephalins, and within the Platycephalus indicus species complex, that coincide with the mid-Miocene glaciation (~10 Ma; Figure 4.5). Cooling throughout the mid to late-Miocene appears to have prompted ancestral P. marmoratus and P. orbitalis to retreat northwards up the eastern and western Australian coasts forming geographically isolated lineages (Figure 4.3b) that now separate along isotherms known to restrict the distributions of other marine groups (O'Hara & Poore 2000). Sister species P. speculator and P. caeruleopunctatus show adjacent distributions converging in Bass Strait that correspond to expectations of allopatric separation (Figure 4.3e). The imprint of the Bassian Isthmus as an intermittent land bridge is similarly evident across a diverse spectrum of marine groups (Waters 2008). However, the distributions of sister species P. bassensis and P. longispinis do not reflect this same vicariant pattern (Figure 4.3d) despite their synchronous divergence with P. speculator and P. caeruleopunctatus (Figure 4.5). A glacial event may have initiated separation in ancestral P. speculator and P. caeruleopunctatus through a vicariant split, with possible parapatric separation along a depth gradient in ancestral P. bassensis and P. longispinis. This form of depth-related parapatric speciation has been proposed for rockfishes (Sebastes) in the absence of any differences in life history, diet or latitudinal geographical separation (Ingram 2011). Competitive exclusion is unlikely to be maintaining postglacial separation in one group and not the other as the allopatrically distributed P. speculator and P. caeruleopunctatus sister species occupy separate depth and habitat preferences. Mode of speciation, ecological and/or oceanographic factors (Dawson 2005; Waters 2008) therefore probably account for these inconsistent postglacial distribution ranges.
4.5.5 The Platycephalus indicus complex
The Platycephalus indicus species complex represents the most comprehensively sampled flathead group across the tropical IWP. The most pronounced divergence; coinciding
with the mid-Miocene climate shift, split the Indian and Pacific Ocean groups along the Sunda Arc and Torres Strait (Figure 4.5). Levels of intra-species divergence across the P. indicus complex are found in other, less well-sampled flathead species across similar geographical locations (Puckridge et al. 2013a), as well as across other, diverse marine groups (Andreakis et al. 2012; Poore & Andreakis 2011; Puckridge et al. 2013b). These observations hint at the potential magnitude of unaccounted for, cryptic diversity across this region and also suggest that processes creating diversification in the P. indicus complex may be acting on whole suites of species.
Distinguishing between geographical fragmentation of widely distributed populations and profuse net speciation among narrowly distributed taxa can be difficult (Jablonski 2007). However, the repeating patterns of species divergences observed across spatial (e.g. Figures 4.2, 4.3c & 4.4) and temporal scales (e.g. Figures 4.2c, d) strongly suggest vicariant isolation and species survival across multiple refugia during glacial coastline contractions. These recovered patterns are consistent with climate-driven centrifugal speciation (Brown 1957), suggesting this process may be a key factor creating diversity in this region (Briggs 2000). As new lineages arise in peripheral and central regions, it is hypothesised that unless peripheral groups develop proper specializations, central lineages will expand and, following dispersal, out-compete peripheral lineages (Brown 1957).
4.5.6 Systematic considerations
Despite the basal position of Ratabulus in the onigociin phylogeny, as originally proposed by Imamura (1996), the subfamilial topologies of his schemes are not in agreement with those presented here. The present study and that of Imamura (1996) infer relationships across the Onigociinae in the absence of a number of its taxa. Therefore the phylogenetic accuracy of inferred relationships within this section of the phylogeny is considered partially compromised due to incomplete sampling (Rokas & Carroll 2005). However, the polyphyletic and/or paraphyletic status of several genera (e.g. Thysanophrys, Onigocia, and Inegocia) is well supported from both nuclear and mitochondrial data and is in conflict with the more recent taxonomic revisions (Imamura 1996). Additionally, equivocal relationships question the monophyly of Cymbacephalus, Sunagocia and Sorsogona. The clade containing
Sorsogona has the least taxonomic coverage, yet S. prionota and S. portuguesa are not grouped with the type species of the genus S. tuberculatus,or with Rogadius, as proposed by Imamura (1996).
At present, the Platycephalinae consists of two genera. Based on anatomical characters, Imamura (1996) placed the monotypic Elates basal to the Platycephalinae, a relationship that was not recovered from the molecular phylogenies. However, the position of
suggesting the need for additional markers to resolve its position. The proposed relationships among Platycephalus speciesin this study are based on the most comprehensive sampling of the genus to date (15 nominal species and 8 additional unnamed taxa), with Imamura (1996) and Keenan (1991) basing their phylogenetic reconstructions on 7 and 12 Platycephalus
species respectively. Proposed Platycephalus relationships by Keenan (1991) are more consistent with those of the present study despite differences in marker choice and reconstruction method.
The decrease in LL scales with decreasing latitude and depth in the platycephalins is consistent with a phenomenon known as Jordan’s Rule (see McDowall 2008 for discussion). This is most widely recognised by number of vertebrae, however correlations with LL scales and branched anal rays have been noted (Hubbs 1922). Temperatures during early development, phyletic position, body shape and swimming mode may be determining factors (McDowall 2008). As mechanisms responsible for these correlations are poorly understood, Platycephalids could represent an ideal candidate for examining causative processes given their broad latitudinal range and their apparent, recent tropical expansion. In addition, while there is a correlation in LL scales, vertebral counts are highly conserved in flatheads (27 vertebrae; Knapp 1999).
4.5.7 Conclusions
The timing and directionality of species diversification in tropical seas represent an expanding field in modern ecology and macroevolution. However, the climatic and evolutionary processes underlying LDGs still remain controversial or cannot be determined with certainty. Molecular phylogenies coupled with molecular clock approximations, can provide a powerful tool for elucidating palaeo-climatic changes and geological events responsible for the distribution of marine taxa across temperate and tropical regions. Given the commercial importance of flatheads and taxonomic uncertainty, the present results have considerable implications for future management and conservation strategies, and provide a comprehensive framework for exploring evolutionary processes in this family.
‘‘the affinities of all the beings of the same class have sometimes been represented by a great tree… As buds give rise by growth to fresh buds, and these, if vigorous, branch out and overtop on all sides many a feebler branch, so by generation I believe it has been with the great Tree of Life, which fills with its dead and broken branches the crust of the earth, and covers the surface with its ever branching and beautiful ramifications.”