On the trail of biodiversification processes

Dans le document New insights into the diversity of deep-sea benthic foraminifera (Page 170-176)

CHAPTER 5: GENERAL DISCUSSION, CONCLUSIONS AND PERSPECTIVES153

5.1.2 On the trail of biodiversification processes

In this section, we will discuss the general patterns of foraminiferal diversity based on the previous discussion. We will speculate here on the general biodiversification processes, which could explain those patterns.

The global genetic homogeneity of E. exigua shown in chapter 4 has considerable consequences on our interpretation of foraminiferal species distribution. By providing evidence for lack of genetic differences between widely distributed populations of this species, we show that benthic foraminifera have the potential ability to disperse globally.

First of all, the role of microhabitat segregations at sediment-water interface could be put forward to explain differences between calcareous species concerning their geographic distribution. E. exigua and C. wullerstorfi are known to have epifaunal life habits and both display rather less biogeographic pattern in their gene structures than O. umbonatus, which is infaunal. It can thus be proposed that juveniles or gametes of epifaunal species may be dispersed in an easier way than infaunal ones, which reproduce in sediment interstices far from currents.

The depth parameter seems to be somehow involved in the separation between species displaying clear biogeography patterns and the others (if E. exigua is not a genuine case). This idea is supported by the important crypticity in shallow water species of Epistominella. Indeed, five cryptic species (E. arctica, E. vitrea, Epistominella sp.1, Epistominella sp.2, Epistominella sp.3) have been found shallower than 1200 m, while apparently only one (E. exigua) occurs deeper. We suspect that the crypticity and the richness of others calcareous species would also tend to decrease with depth. However, we do not exclude the possibility that other species of the genus Epistominella could occur in the deep-sea neither that some of them could present limited geographic distribution. We propose that this feature of ubiquity increasing with depth would be rather a tendency than a common trend or general law. Moreover, we do not believe that the depth could act as a physical constraint restricting the dispersal and we even doubt that it could be directly correlated with species richness. We rather suspect that the dispersal and crypticity patterns would be linked to other parameters such nutrient concentration, which often depend on depth.

If we consider, once again, the different trophic strategies between species of benthic foraminifera, we could schematically distinguish the highly specialized taxa from the opportunist ones. As we proposed in the introduction, monothalamous species present many specialized traits in their highly adapted morphologies. They are also the most ancient group of foraminifera and probably the richest one in the deep-sea environment. In contrast, the polythalamous calcareous rotaliids include typical opportunist species, such as E. exigua, which are able to bloom rapidly where nutrients become abundant. The rotaliids are much younger in the evolutionary history of benthic foraminifera. They also display less genetic diversity than that found within monothalamous species, at least considering our database of the SSU rDNA sequences. All these observations converge to the following evolutionary scenario:

Hypothetically, deep-sea monothalamous foraminifera would have diversified by adaptation to different environments as well as by niches partitioning at the same location.

The deep sea offer many oligotrophic places of relative stability, where a niche partitioning is especially likely to occur. Monothalamids specialization might have been enhanced by the facility to acquire or to lose an agglutinated test, occurring independently in different lineages.

Indeed the extremely wide range of morphologies found in this group, offers numerous

possibilities of adaptation to a great variety of ecological niches. This remark would be even more relevant for those agglutinated monothalamids, which selectively pick up different particles from local environment and enhance in this way their diversification potential. It is thus plausible that a strong positive selection occurred in deep-sea monothalamous foraminifera regarding the features of their test that could explain the high evolution rates and the high richness of this group.

In the case of deep-sea rotaliids, a hypothesis would be that some of them, like E.

exigua, changed their trophic strategy toward opportunism. In the deep sea, the opportunist taxa with generalist trophic behaviour should logically be favoured. Indeed, large food inputs are ephemeral and often unpredictable. It should therefore be convenient for a species to be able to feed on a wide range of resources and take benefit from a maximum of food opportunities. The generalist behaviour could also diminish the impact of food niche partitioning as diversification factor. Hotspots of resources in the deep-sea are thought to last not long enough for local populations to reach a steady state and start to compete between each others. Without competition, niches partitioning seems quite unlikely. This could provide explanation of the relatively slow diversification of opportunist taxa. Nevertheless, evolution rates highly depend on species dispersal and the geographic distribution should be taken into account.

We believe that deep-sea benthic foraminifera have globally considerable physiological ability for dispersal. For instance, most of them are small enough to be carried by currents on long distances. There are also evidences that they can construct cysts and adopt a dormant state (Heinz et al., 2005), which could potentially allow them to survive during long transportation despite food deprivation and changing physico-chemical conditions. The causes of their geographic occurrence at regional scale should thus be searched according to their ecological “interest” rather than to their ability to disperse. The point is probably not to know whether they could reach a given area but rather to predict whether that area is sufficiently attractive for them to settle there. Considering the opportunist trophic strategy, we could expect that deep-sea multi-chambered calcareous species, such as E. exigua, would have considerable interest to be widely dispersed, since they need to follow the resources hotspots where they appear. The patchier these hotspots are, the more widely dispersed opportunist species should be. Yet, the patchiness of resources is supposed to increase with

the oligotrophic character of environment and thus with the depth. For that reason, it would not be surprising that the dispersal potential of opportunist taxa would increase with depth.

The distribution of Epistominella species, which seems to get wider with depth, would thus reflect a way to cope with an increasing patchiness of food resource. A wide dispersal should increase the gene flow and contribute to reduce diversification rates.

Additionally, it could be proposed that the diversification of opportunist species by food niches partitioning would also affect their distribution. Differences between resource types are obviously greater in shallow water than in the deep sea. Most of the food available for opportunist deep-sea foraminifera consists in decomposed organic matter (such as phytodetritus) coming from upper layers. In the deep sea, it is likely that this kind of resource would differ globally with depth rather than with geographic location inducing a vertical speciation rather than a horizontal one. Opportunist species living sufficiently deep should generally face similar type of nutrients and would have therefore fewer possibilities to speciate by “food partitioning”. This could possibly contribute to increase their geographic ubiquity with depth.

The gene flow of E. exigua prevails on its diversification rate but its populations display a relatively high variability, as indicated by multiple single point mutations present in their SSU and ITS rDNA. This could reflect a fast evolution of the ribosomal genes in this species. However, we may also think that this is related to the fact that the wide dispersion and the global gene flow of E. exigua are actually recent. A hypothesis would be that this species has improved its dispersal potential and shifted toward a more opportunistic trophic strategy. Genetically distinct populations of E. exigua would thus have been propagated quite recently and mixed between each others. The high genetic variability would thus be the trail of a previous biogeographic isolation.

The cosmopolitanism of E. exigua remains remarkable even if it would constitute an exception. We suspect, however, that other deep sea benthic species could also display a global genetic distribution although they should not be numerous since opportunistic way of life does not promote biodiversification. The number of ubiquitous foraminiferal species could be thought, at first glance, to be somehow correlated with the total amount of available providential nutrient such as phytodetritus. Indeed, even without a strong niche partitioning by food, opportunist species sharing the global resources should slowly separate until their

populations become small and follow stochastic model where there is equilibrium between species (see section 1.1.2). At evolutionary scale, a higher amount of global resources should thus result in a higher richness of ubiquitous species. In a certain way, diversification processes in opportunist taxa, such as E. exigua, could be compared to those described by Pedros-Alio for microorganisms (see Fig. 1.2.2). As microbes, they tend to be globally dispersed and could also be separated into dominant and rare species respectively. At a certain time and locality, the dominant opportunist species would be flourishing on providential hotspots, while rare opportunist species would “wait” the environmental change, which would favor them and allow their population to increase. It is for instance possible that E. exigua was some time ago a rare species, which became once and is until now successful. As for microbes, opportunist species should not get easily extinct since they can supposedly feed on a wide range of food and should have high dispersal ability: at least few representatives of a rare species should find enough food to survive. For all these reasons, we expect relatively few deep-sea benthic foraminifera with a current global distribution but a high number of species, which could potentially become ubiquitous. The richness of those opportunist taxa should be increasing with time.

Finally, foraminifera would encompass two different kinds of deep-sea “specialists".

The first one would comprise mostly monothalamous taxa, highly adapted to oligotrophic local environments. They would be older, diversify relatively fast thanks primarly to their wide range of tests and should consist in the main part of foraminiferal richness. The second kind would include the opportunist and generalist taxa, especially adapted to the patchiness of deep-sea food resources. Some of the dominant species may have a global dispersal, while the other rare ones wait for better times. This kind of “opportunist deep-sea specialists” would slowly diversify thanks to a trophic strategy preventing them from extinction. This foraminiferal model could possibly fit to other eukaryotes including big metazoans. Indeed, these two schematic biodiversification pathways could evoke the differences existing between other deep-sea ecosystems. For instance, pelagic organism highly adapted to oligotrophy versus hydrothermal vents fauna coping with patchy and abundant resources of short availability.

Dans le document New insights into the diversity of deep-sea benthic foraminifera (Page 170-176)