Origen y evolución de la Familia Eoglobigerinidae Blow, 1979, de foraminíferos planctónicos durante el Daniano inferior (Paleoceno)

Ignacio Arenillas* and José Antonio Arz

Departamento de Ciencias de la Tierra (Paleontología) and Instituto Universitario de Investigación en Ciencias Ambientales de Aragón, Universidad de Zaragoza, C/Pedro Cerbuna 12, E-50009 Zaragoza, Spain. *ias@unizar.es

Manuscript received: July 23, 2012 ]]> Corrected manuscript received: November 9, 2012
Manuscript accepted: November 12, 2012

RESUMEN

Nuevas evidencias sobre el origen y diversificación de la Familia Eoglobigerinidae Blow, 1979, o linaje reticulado-espinoso de foraminíferos planctónicos del Paleoceno, han sido identificadas en algunas de las secciones más continuas del Daniano inferior, principalmente en El Kef y Aïn Settara (Túnez). El descubrimiento de ejemplares transicionales sugiere una evolución desde el ancestral género Palaeoglobigerina Arenillas, Arzy Náñez, 2007 (depared lisa) hasta Eoglobigerina Morozova, 1959 (de pared reticulada), y desde éste último hasta los géneros Parasubbotina Olsson, Hemleben, Berggren y Liu, 1992 y Subbotina Brotzen y Pozaryska, 1961. La transición entre Palaeoglobigerinay Eoglobigerina implica cambios texturales progresivos en la superficie de la pared, tales como el desarrollo de poros en copa, espinas y finalmente pared reticulada. Este tránsito, sin embargo, implica cambios morfológicos externos pequeños entre la especie ancestral Palaeoglobigerina fodina (Blow, 1979) y la descendiente Eoglobigerina simplicissima (Blow, 1979), como son el incremento en el tamaño de la concha y del espesor del labio apertural.

Palabras clave: Paleoceno, textura de la pared, espinoso, eoglobigerínido, filogenia.

ABSTRACT

New evidence on the origin and diversification of the plankticforaminiferal Family Eoglobigerinidae Blow, 1979, or Paleocene spinose, cancellate lineage, has been discovered from some of the most continuous lower Danian sections known to date, especially from El Kef and Aïn Settara (Tunisia). Based on the discovery of transitional specimens, we suggest an evolution from primitive, smooth walled Palaeoglobigerina Arenillas, Arz and Náñez, 2007, to cancellate Eoglobigerina Morozova, 1959, and then on to Parasubbotina Olsson, Hemleben, Berggren and Liu, 1992, and Subbotina Brotzen and Pozaryska, 1961. The transition from Palaeoglobigerina to Eoglobigerina implied progressive textural changes in the wall surface, such as the development of pore-pits, spines and eventually a cancellate wall. This transition, however, implied minor external morphologic changes between ancestral Palaeoglobigerina fodina (Blow, 1979) and its descendant Eoglobigerina simplicissima (Blow, 1979), such as the increase in test size and the thickness of the apertural lip.

Key words: Paleocene, wall texture, spinose, eoglobigerinid, phylogeny.

INTRODUCTION

The wall structure of the test of the earliest Danian planktic foraminifera underwent major changes after the Cretaceous/Paleogene (K/Pg) mass extinction event (Liu and Olsson, 1992, 1994). These changes resulted in the evolution of four wall textures among the trochospiral plank-tic foraminifera which became more or less stable during the early Danian: spinose cancellate wall (Eoglobigerina Morozova, 1959; Subbotina Brotzen and Pozaryska, 1961; and Parasubbotina Olsson, Hemleben, Berggren and Liu, 1992), nonspinose cancellate wall (Praemurica Olsson, Hemleben, Berggren and Liu, 1992), pitted-smooth wall (Globanomalina Haque, 1956), and pustulate wall (Globoconusa Khalilov, 1956). The spinose cancellate lineage is included in the Family Eoglobigerinidae Blow, 1979. The spinose wall indicates a carnivorous regime. Among the planktic foraminifera, this lineage was probably the first to occupy this niche in the earliest Paleocene (Olsson et al., 1999). During the reproductive process (gametogenesis) the spines are dissolved, leaving holes in the empty spine, which are only visible with the help of a scanning electron microscope (SEM), if the preservation is good enough.

The origin of the spinose lineage during the earliest Danian is uncertain, although several phylogenetic hypotheses have been advanced. Olsson et al. (1992) and Liu and Olsson (1994) proposed that the "normal" perforate Danian planktic foraminifera (i.e., pitted and cancellate walls) derived from Hedbergella Brönnimann and Brown, 1958. This hypothesis was already proposed by Berggren (1962, 1977), Olsson (1963, 1970) and Blow (1979). Olsson et al. (1992, 1999) suggested H. monmouthensis Olsson, 1960, as the predecessor of the spinose lineage. Apellaniz et al. (2002) also suggested a hedbergellid origin for the spinose lineage but they considered Hedbergella hillebrandti Orue-Extebarria, 1985, as the ancestral form. In contrast to these, Arenillas and Arz (1996, 2000) and Arenillas et al. (2010) proposed that Palaeoglobigerina Arenillas, Arz and Náñez, 2007, was the ancestor of Eoglobigerina and, therefore, of the spinose lineage.

In this paper, we have documented specimens with intermediary morphologically and texturally features from the smooth-walled Palaeoglobigerina to spinose cancellate walled Eoglobigerina, and from the latter to Parasubbotina and Subbotina. This study is based on high-resolution biostra-tigraphy and an intensive search for transitional specimens between species and genera in nine lower Danian sections of Europe, the Americas and North Africa, and in the Deep Sea Drilling Project Site 305 (Shatsky Rise, North Pacific).

MATERIAL AND METHODS

Because they are two of the most continuous and expanded lower Danian sections known to date (Molina et al. 2006, 2009), this work is focused especially on El Kef and Aïn Settara sections (Tunisia). These sections allowed us to establish with precision the level of the first stratigraphical occurrences of studied species and genera. Figure 1 shows the biostratigraphic ranges of the studied taxa during the first 480 ky of the Paleocene, as well as the correlation of the zonations of Arenillas et al. (2004) and Berggren and Pearson (2005).

The zonation by Arenillas et al. (2004) includes six subzones: Hedbergella holmdelensis and Parvularugoglobigerina longiapertura Subzones of the Guembelitria cretacea Zone, the Parvularugoglobigerina sabina and Eoglobigerina simplicissima Subzones of the Pv. eugubina Zone, and the Eoglobigerina trivialis and Subbotina triloculinoides Subzones of the P. pseudobul-loides Zone. As shown in Figure 1, the Zone P0 of Berggren and Pearson (2005) is equivalent to the H. holmdelensis Subzone, the Zone Pα approximately spans both P. longia-pertura Subzone and Pv. eugubina Zone, and P1a and P1b are roughly equivalent to E. trivialis and S. triloculinoides Subzones respectively. In order to study taxonomic details, we also have revised the fossil material from Elles (Tunisia), Ben Gurion (Israel), Caravaca and Agost (Spain), Bajada del Jaguel (Argentine), Lynn Creek (Mississippi) and Deep Sea Drilling Project Site 305 (Shatsky Rise, North Pacific). In addition, the biostratigraphic scheme proposed in Figure 1 takes also into account other relevant K/Pg sections, such as Gubbio (Italy), Zumaia (Spain), Bidart (France), El Mulato, El Mimbral, La Lajilla, Bochil and Guayal (Mexico), and Loma Capiro (Cuba). Geographical coordinates of all strati-graphic sections are given in Appendix 1.

All samples were disaggregated in water with diluted H₂O₂, and washed through a 63-µm sieve. SEM-photographed specimens were mainly chosen from the El Kef and Aïn Settara sections. Although the diagenesis-induced recrystallization can be seen in many specimens of the Tunisian sections ("frosty" specimens according to the terminology of Sexton et al., 2006), state of preservation is good enough to allow the analysis of the wall texture to be analyzed. Wall textures were examined under scanning electron microscopes JEOL JSM 6400 and Zeiss MERLIN FE-SEM at the Electron Microscopy Service of the Universidad de Zaragoza (Spain). Over 650 SEM-photographs, including different views and details of the surface of the tests of 180 specimens, were taken. Some of them are transitional morphotypes between two species. With the exception of the illustrations of type-specimens copied from the publications of other authors, all the specimens illustrated in Figures 2-9 (3, 4, 5, 6, 7, 8) are deposited in the Departamento de Ciencias de la Tierra of the Universidad de Zaragoza (Spain).

TAXONOMIC AND PHYLOGENETIC NOTES ON EOGLOBIGERINIDS AND RELATED GENERA

The classification used for the eoglobigerinids and their ancestral forms as recognized in this paper is mainly based on those by Blow (1979), Toumarkine and Luterbacher (1985), Olsson et al. (1992) and Arenillas (1996), with some modifications and updates of Olsson et al. (1999) and Arenillas et al. (2007). The following species were analyzed: Palaeoglobigerina alticonusa (Li, McGowran and Boersma, 1995; Figures 2.1-2.2), Pg. fodina (Blow, 1979; Figures 2.3-2.5), Eoglobigerina simplicissima Blow, 1979 (Figures 2.6-2.9), E. eobulloides Morozova (1959; Figures 2.10-2.13), E. praeedita Blow (1979; Figures 2.14-2.16), E. edita (Subbotina, 1953; Figures 2.17-2.20), E. cf. trivialis (E. trivialis Subbotina, 1953, sensu Blow, 1979; Figures 3.1-3.7), E. microcellulosa (Morozova, 1961; Figures 3.8-3.10), E. fringa (Subbotina, 1950; Figures 4.1-4.3), Subbotina triloculinoides (Plummer, 1927; Figures 3.113.15), Parasubbotina moskvini (Shutskaya, 1953; Figures 4.4-4.6), P. varianta (Subbotina, 1953; Figures 4.7-4.9) and P. pseudobulloides (Plummer, 1927; Figures 4.10-4.12). Apellaniz et al. (2002) used a similar taxonomic scheme for the eoglobigerinids. Diagnostic characteristics of all these species are presented in Appendix 2. Details of the wall surface of selected species are illustrated in Figures 5-9 (6, 7, 8).

The discrimination of these species is not supported by morpho- or ecostatistical analyses, therefore some of them can be synonyms. Nevertheless, we retain this classification to analyse better the relationships between taxa, since some of them are intermediate forms between three to four-chambered Eoglobigerina and four to six-chambered Eoglobigerina (e.g., E. eobulloides), between Eoglobigerina and Parasubbotina (e.g., E. fringa), and between Eoglobigerina and Subbotina (e.g., E. microcellulosa). Parasubbotina moskvini was not considered by either Olsson et al. (1999) nor Apellaniz et al. (2002), and most probably they included it in P. varianta. Others assigned it to P. pseudobulloides (e.g., Stainforth et al., 1975; Blow, 1979; Toumarkine and Luterbacher, 1985). Arenillas (1996) restricted the name "varianta" to morphotypes with four chambers in the last whorl and a high rate of chamber size increase, and "pseudobulloides" to morphotypes with more than four chambers (usually between 4 V to 5 chambers), and retained the name "moskvini" for morphotypes that also have four chambers in the last whorl as "varianta" but only a moderate to low rate of increase in chamber size.

The Family Eoglobigerinidae was defined by Blow (1979) for the Paleogene globigerinids with trochospiral coil, an essentially intraumbilical (or asymmetrically umbilical) aperture with a porticus (i.e., thick lips), and cancellate wall texture (i.e., pore-pits and associated interpore ridges). Initially he included the genera Eoglobigerina, Subbotina, and Globastica Blow, 1979 in this family, and considered the first two genera to be phylogenetically related, whilst the third collaterally related to Eoglobigerina. He also suggested that genera Eoglobigerina and Globastica contain taxa probably derived paedomorphically from Cretaceous rugoglobige-rinid ancestors. Contrary to the opinion of Blow (1979), Globastica is now widely considered to be a junior synonym of Globoconusa Khalilov, 1956 (Olsson et al., 1999). Moreover, Globoconusa (= Globastica) must be excluded from the Family Eoglobigerinidae as its wall texture is more closely related to the Family Guembelitriidae Montanaro-Gallitelli (1957), as proposed Olsson et al. (1999).

Loeblich and Tappan (1987) emended the Family Eoglobigerinidae, suggesting its member to have a non-spinose smooth or pitted wall instead of cancellate wall. They included the smooth-walled genus Parvularugoglobigerina Hofker (1978) and excluded the genus Subbotina, which was reassigned to the Family Catapsydracidae Bolli, Loeblich and Tappan, 1957. Olsson et al. (1992, 1999) re-included Eoglobigerina and Subbotina in the Family Globigerinidae Carpenter, Parker and Jones, 1862, where it had been placed traditionally (Subbotina, 1953; Bolli, 1957; Berggren, 1977), and added their recently defined genus Parasubbotina to the same family. Furthermore, they moved Parvularugoglobigerina to the Family Guembelitriidae because of the close relationships between parvularugo-globigerinids and guembelitrids.

The species of the genus Palaeoglobigerina are usually grouped in Parvularugoglobigerina, as both genera have an identical wall texture (Arenillas et al., 2007, 2010). They exhibit a smooth wall texture with tiny pore-murals (< 1 µm in diameter). Arenillas et al. (2007) separated Palaeoglobigerina, whose type-species is Pg. fodina (Blow 1979; Figures 2.1-2.3), from Parvularugoglobigerina, whose type-species is Pv. eugubina (Luterbacher and Premoli-Silva, 1964), to comprise species previously classified as primitive Eoglobigerina or Globoconusa (Blow, 1979; Canudo et al., 1991; Keller, 1988; Keller et al., 1995; Arenillas and Arz, 1996, 2000). Palaeoglobigerina differs from Parvularugoglobigerina by its smaller number of chambers, both in the first spire whorl (3 ½ - 4 instead of 4 - 4 V) and in the last one (3 - 4 instead of 4 - 9). However, both genera are closely related, are included into an informal "parvularugoglobigerinid" group, and seem appropriate to be classified within the Family Guembelitriidae (Olsson et al., 1999). The inclusion of parvularugoglobigerinids such as Palaeoglobigerina in the Family Eoglobigerinidae, as done by Loeblich and Tappan (1957) and Apellaniz et al. (2002), is debatable because they present sharply different wall texture.

Arenillas et al. (2012) have recently revealed the occurrence of two groups of primitive trochospiral species with different wall textures and stratigraphic ranges in the earliest Danian. The first group, whose species were attributed to parvularugoglobigerinids, exhibits a smooth wall texture (with pore-murals) and evolved in the proximity of the P0-Pα transition. The second group, assigned to the new genus Trochoguembelitria Arenillas, Arz and Náñez, 2012, has a rugose wall texture (with rugosities and irregular pore-mounds) and evolved in the proximity of the Pα-P1 transition. Textural and biostratigraphic data suggest that this group is a lineage different from that of the parvularu-goglobigerinids. Trochospiral specimens with rugose or pore-mounded wall were already documented by Liu and Olsson (1992, 1994), and Olsson et al. (1992, 1999), but they considered them as belonging to Guembelitria?, or to Parvularugoglobigerina after emending the genus. It is important to consider this aspect because the smooth wall type attributed to parvularugoglobigerinids should not be misinterpreted as a product of poor preservation in the tunisian sections, since specimens with smooth wall and others with more ornamented walls (i.e., pore-mounded Guembelitria, and/or rugose Woodringina) cooccur in the samples from the P0-Pα transitional interval similarly affected by the diagenesis process (Arenillas et al., 2010, 2012).

Eoglobigerina, whose type-species is E. eobulloi-des, was initially defined as a subgenus of Globigerina and described as Danian globigeriniforms with a thin and smooth wall (Morozova, 1959). Blow (1979) emended Eoglobigerina, elevating it to generic rank and re-describing it to have a cancellate wall texture (pore-pits usually with clearly defined interpore ridges), intraumbilical aperture with a weakly developed porticus (i.e., thick lip). He also suggested that it represents a primitive group ancestral to Subbotina Brotzen and Pozaryska, 1961. Blow (1979) tentatively included some earliest Danian species with smooth wall in Eoglobigerina?, such as E.? fodina (Blow, 1979) or E.? extensa (Blow, 1979), reassigned later to Palaeoglobigerina by Arenillas, Arz and Náñez (2007). Hemleben et al. (1991) demonstrated that Eoglobigerina has a spinose texture, which clearly separates it from the other cancellate taxa such as Praemurica. For this reason, Olsson et al. (1999) emended the genus to include the spinose character.

Parasubbotina, whose type-species is P. pseudobul-loides, was defined to group low trochospiral, spinose-can-cellate globigeriniforms of the Danian (Olsson et al., 1992). Its aperture was described as umbilical-extraumbilical and bordered by a narrow lip. As in other eoglobigerinids, the degree of development of the cancellate wall varies from one specimen to another, probably depending on the paleoenvi-ronmental conditions. These species, mainly P. moskvini and P. pseudobulloides, display a weakly developed cancellate wall in the transition between the Pv. eugubina and the P. pseudobulloides Zones. Therefore, it is often difficult to recognize the first occurrence of both species, and consequently the base of the P. pseudobulloides Zone. For this reason, Olsson et al. (1992, 1999) proposed the species Parasubbotina aff. pseudobulloides to comprise such small primitive morphotypes.

DISCUSSION

According to Arenillas et al. (2007) the first species to evolve of Eoglobigerina, Parasubbotina and Subbotina were E. simplicissima, P. moskvini and S. triloculinoides respectively. Intermediate specimens between these taxa have been found mainly in lowermost Danian samples of El Kef and Aïn Settara. Figures 5-9 (6, 7, 8) illustrate details of the wall surface of some of these specimens, which suggest an evolution of the wall texture as proposed in Figure 10.

Some of the SEM-photographed specimens display characteristics transitional between Pg. fodina and E. simplicissima (Figures 5.4-5.5; Figures 6.1-6.2). The external morphology of both species is very similar, differing mainly in the shape of the aperture, the thickness of the lip and the test size. Typical Pg. fodina exhibits a highly arched aperture with a thin lip, although the apertural arch is lower and the lip is thicker in some more modern specimens (e.g., Figures 2.5). In contrast, the test of E. simplicissima is larger and the aperture is a low arch usually with thick lips. The most significant difference between the two species is the wall texture: the first one presents smooth wall, and the second one, pitted or cancellate wall.

The transition from Palaeoglobigerina to Eoglobigerina seems to have implied the following evolutionary changes: (1) increase in test size; (2) increase in pore size; (3) increase in lip thickness; (4) evolution from tiny pore-murals to large pore-pits; (5) development of spines; and (6) evolution from smooth to cancellate wall. The increase in test size and pore size started within the genus Palaeoglobigerina (Figures 5.1-5.3), as exemplified in Figures 10a and 10b. The more primitive specimens of E. simplicissima (Figures 6.4-6.5) are only slightly larger than their ancestor Pg. fodina. However, they are assigned to E. simplicissima because they have incipient pore-pits and thicker lips. The wall texture of these first Eoglobigerina specimens may best be described as pitted (as in Figures 10c, 10d and 10e) rather than as cancellate. Distinct spine holes in these specimens were not visible, but some small holes may be identified in test surface of slightly more modern specimens of E. simplicissima and they could be vacated spine holes (Figures 6.1-6.2). The development of spines seems to have occurred later than the pore-pits, but prior to the development of the cancellate wall as suggested in the diagrams shown in Figures 10e and 10f.

This hypothesis on the origin of the eoglobigerinids, or spinose lineage, differs from those by Olsson et al. (1992, 1999) and Apellaniz et al. (2002) who suggested an early "hedbergellid" origin, occurring shortly after the K/Pg boundary, i.e., within the Zone P0 or H. holmdelensis Subzone. Olsson et al. (1999) suggested major changes in wall texture and test morphology in the transition from the pustulose, pitted H. monmouthensis to the spinose, cancellate Eoglobigerina and Parasubbotina taking place in a relatively short time on a geological and evolutionary time scale. However, we did not find single cancellate specimen assignable to the eoglobigerinids in the Zone P0 at the most continuous K/Pg sections known to date (Arenillas et al., 2000a,b). The Zone P0 was originally defined as the interval between the K/Pg boundary mass extinction and the first occurrence of Danian species (Smit, 1982), i.e., from the last occurrence of upper Maastrichtian Abathomphalus mayaroensis (Bolli, 1951) to the first occurrence of Pg. alticonusa and/or Pv. longiapertura (= Pv. eugubina for other authors). As noted by Arenillas et al. (2004), this original definition of the Zone P0 seems to exclude the occurrence of the eoglobigerinids within it. According to our biostratigraphic data (Figure 1), eoglobigerinids appeared at the time equivalent to the base of the E. simplicissima Subzone (or middle part of Zone Pa). Biostratigraphic and textural data suggest that the evolutionary transition from Palaeoglobigerina to Eoglobigerina is more consistent with our data than the postulated transition from Hedbergella to Eoglobigerina. This scenario involves a smaller number of morphological and textural changes, and is more compatible with the planktic foraminiferal assemblages identified in the Zone P0 and the lower part of Zone Pa, where only triserial and biserial guembelitriids and smooth walled parvularugoglobigerinids were identified (Luterbacher and Premoli Silva, 1964; Smit, 1982; Toumarkine and Luterbacher, 1985; Arenillas and Arz, 2000; Arenillas et al., 2007, 2010).

The very weakly developed cancellate wall (pitted wall) in the earliest representatives of the genus Eoglobigerina, within the E. simplicissima Subzone and the lower part of P. pseudobulloides Zone, contrasts with the strongly developed cancellate wall of the most modern specimens. Some examples of specimens with pitted wall are illustrated, e.g., E. simplicissima (Figures 6.1-6.2) and P. moskvini (Figure 8.3). Olsson et al. (1992, 1999) included these latter morphotypes in P. aff. pseudobulloides, and their wall texture resembles that of the pitted smooth wall of the genus Globanomalina. However, all eoglobigerinids, except perhaps in the earliest specimens of E. simplicissima mentioned above, have already a more or less developed spinose wall texture. In almost all species, the thickness of the lips increases gradually and it resembles a porticus in some specimens of Parasubbotina (e.g., Figures 4.6 and 4.12) and mainly of Subbotina (Figures 3.12-3.13).

The eoglobigerinid spinose lineage is characterized by 3 ½ - 5 chambers in the first whorl (neanic stage). This character separates them from other pitted and cancellate Paleocene taxa such as Globanomalina or Praemurica (5 - 6 neanic chambers). This difference is similar to that which allowed Arenillas et al. (2007) to separate Palaeoglobigerina (3 ½ - 4 neanic chambers) from Parvularugoglobigerina (4 - 4 ½ chambers, or even 5 in the neanic stage). The most primitive specimens of E. simpliccissima (e.g., Figure 5.4) still exhibit 3 ½ - 4 neanic chambers, similarto Palaeoglobigerina (Arenillas et al., 2007). This ontoge-netic trait newly suggests that the eoglobigerinids derived from Palaeoglobigerina, with only a slight increase in the number of chambers in the neanic stage. This character was retained in the eoglobigerinids with 3 ½ - 4 chambers in the last whorl, such as E. microcellulosa (e.g., Figures 3.8-3.10) and E. cf. trivialis (e.g., Figures 3.5-3.6), as well as in Subbotina species (e.g., Figure 3.15).

By contrast, E. fringa, species of Eoglobigerina with more than 4 chambers in the last whorl (E. eobulloides, E. praeedita, and E. edita) and Parasubbotina usually have 4 -5 neanic chambers. Examples of this feature can be observed in Figures 2 and 4. We consider the Parasubbotina lineage (E. fringa - Parasubbotina) and the E. edita lineage (E. eo-bulloides - praeedita - edita) as two separate lineages with E. simplicissima as the common ancestor. They represent two evolutionary trends within Eoglobigerinidae: the first one towards the migration of the aperture in the umbilical-extraumbilical position and a lower trochospire, and the second one towards raising of the trochospire, the increase in the number of chambers and consequently a slower rate in increase of the chamber size.

According to these data, we suggest that four eoglo-bigerinid lineages emerged from E. simpliccissima (Figure 11). The oldest one is the E. eobulloides - E. praeedita - E. edita lineage, which culminates with eoglobigerinids with more than four chambers in the final whorl (Figure 7). This evolutionary series was also suggested by both Olsson et al. (1992, 1999) and Apellaniz et al. (2002). The second one to occur was the lineage that culminated with Parasubbotina, i.e., the evolution from E. fringa to P. moskvini (see Figure 8), and then to P. pseudobulloides and P. varianta. Intermediate specimens between P. moskvini and P. pseudobulloides (e.g., Figure 8.5) and between P. moskvini and P. varianta (e.g., Figure 4.6) are also found. A similar proposal was made by Apellaniz et al. (2002) who also suggested E. fringa as the ancestral form of Parasubbotina. Olsson et al. (1999) concluded that P. aff. pseudobulloides was the ancestral form of this genus. This is consistent with our proposal since they assigned primitive, non-cancellate P. moskvini and P. pseudobulloides to their P. aff. pseudobulloides (see comments above). The third lineage to appear led to the genus Subbotina (see Figure 9) by the evolution from E. microcellulosa to S. triloculinoides. Due to different taxonomic interpretations, Olsson et al. (1999) proposed E. trivialis as ancestor of Subbotina while Apellaniz et al. (2002) suggested E. appressa Blow (1979). However, all the latest hypotheses suggest that Subbotina evolved from Eoglobigerina. Finally, the fourth lineage started with E. cf. trivialis. The evolutionary relationships of this lineage, which tended towards the raising of the trochospire (culminating with E. tetragona Morozova, 1961, in lower-middle Danian), are not so clear at the present state of knowledge. Probably E. cf. trivialis and E. eobulloides share E. simpliccissima as common ancestor, because, as mentioned above, they all present 4 - 5 neanic chambers occasionally.

CONCLUSIONS

An intensive search of transitional specimens, mainly from the lower Danian El Kef and Aïn Settara sections, has allowed us to find new evidence on the origin and early diversification of the Family Eoglobigerinidae, which groups together spinose and can-cellate genera of the early Paleocene (e.g. Eoglobigerina, Parasubbotina and Subbotina). Our data suggest an evolution from Palaeoglobigerina to Eoglobigerina, and then in separate branches to Parasubbotina and to Subbotina.

The transition between Palaeoglobigerina and Eoglobigerina implied an increase of the test size, the pore diameter and the thickness of the lip, as well as the development of pore-pits, spines and, finally, cancellate walls. At least four lineages derived from E. simplicissima:

(1) Parasubbotina Lineage (E. fringa, P moskvini, P. varianta, P. pseudobulloides) tending towards the migration of the aperture into an umbilical-extraumbilical position, and a lower trochospire;

(2) Subbotina Lineage (E. microcellulosa, S. triloculinoides), tending towards a decrease in the number of chambers and a higher rate of increase in the chamber size;

(3) E. edita Lineage (E. eobulloides, E. praeedita, E. edita), tending towards the trochospire raise, the increase in the number of chambers and a lower rate of chamber size increase;

(4) E. cf. trivialis Lineage, tending towards the trochospire raise.

ACKNOWLEDGMENTS

We thank Hanspeter Luterbacher, and an anonymous reviewer for helpful comments. We also thank Carolina Náñez for the review of the manuscript. This research was funded by the Spanish Ministerio de Ciencia e Innovation projects CGL2011-23077 and CGL2011-22912 (both co-financed by the European Regional Development Fund), and the Aragonian Departamento de Educacion y Ciencia (DGA group E05). Authors would like to acknowledge the use of Servicio General de Apoyo a la Investigacion-SAI, Universidad de Zaragoza.The authors are grateful to Richard Stephenson for English corrections.

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