J.H. Huber *
A comprehensive and detailed comparison of Old World and New World tropical Cyprinodonts (oviparous Cyprinodontiformes, Pisces) is proposed, based on the most recent knowledge in paleogeography and palynology. It covers biogeographical aspects, from the analysis of a data base of over 3500 localities-species in tropical countries (Huber, 1996) of Africa, America and Indo-Asia (fig. 1, with local country names). It synthetizes, with a novel transversal perspective, the already published information by the author, since 1978, and by others, on systematics, genetics, external morphology, live coloration, behavior and ecology of tropical Cyprinodonts, to emphasize the many similarities and the few differences. The many similarities are hypothesized to be the result, from a process of convergence after the continental drift, of the limited capacity of these reclusive fishes, quasi exclusive in their highly uncertain biotopes, to produce a diversity of responses in the face of similar environmental changes.
Several novel biogeographical and evolutionary models are hypothetically proposed for the first time for Cyprinodonts, to replace those which failed, like the present types of soil, the present river basin outlines (… ), all featuring today characteristics.
All these models refer to past periods and notably the dramatic climatic changes of the Quaternary. They explain and correlate well with our present knowledge on Cyprinodont in the New and Old Worlds:
Schematically, a two-scaled evolutionary history of these fishes is hypothetically proposed. One, old, for the creation and diversification of the major morphotypes along millions of years. Another, recent, along thousands of years only and linked to climatic disorders, for the explosion of the genotypes and a vicariant speciation from slightly different morphotypes which had not suffered a previous extinction.
In our Review of Rivulus (1992: 50), after having studied in depth all groups of Cyprinodonts from tropical Africa and America (since 1978, op. cit.), we emphasized the similarity in basic phenotypes, that were available both in the Old World and the New World, with 3 profiles:
No sure component was available in the New World, at that time.
However, one species with a decided similarity with Aplocheilus, but annual, was subsequently discovered in the Paraguayan Chaco. It was then described and named Trigonectes aplocheiloides Huber, 1995.
Fig. 2. The still single Gondwana continent (148 MYA), origin of the Aplocheilids and Aplocheilichthyins. Note that the hypothetical position of the Madagascar-India block is attached to Antarctica and maintained that way after the African drift. This hypothesis is different from the more traditional position of that block, with the southern part of Madagascar being attached to Africa at the level of Tanzania (modified from Smith et al., 1994). Primitive (by external characters) morphotypes, Aplocheilids: 1.Pachypanchax; 2.Aplocheilus panchax; 3.Aplocheilus lineatus et al.; 4.Callopanchax; 5.Rivulus caudomarginatus; 6.Paranothobranchius; 7.Cynolebias s.s.; 8.Millerichthys; 9.Austrofundulus-Rachovia-Pituna; 10.Fundulopanchax. Aplocheilichthyins: 11.Pantanodon; 12.Lamprichthys; 13.Laciris; 14.Aplocheilichthys s.s.; 15.Micropanchax s.s.; 16.Fluviphylax.
In addition, we dedicated a chapter of that book (1992: 51) to the parallel comparison of the major characteristics of the genera Rivulus of the New World and Aphyosemion of the Old World, in a synthetic way. The many disclosed similarities induced, in conclusion (1992: 54), two possible schematic explanations:
Osteological studies with a cladistic approach (Parenti, 1981; Costa, 1990) had already favored the second explanation by exemplifying only 2 ancestors, one for each continent. But cladistics were not universally accepted in those days and these studies were first based on very limited material. In addition, they placed annual forms as derived from non annuals, which we did not follow (Huber, 1996).
It was only in 1997 that Murphy & Collier (op. cit.) were able to demonstrate by the molecular analysis of three genetic fragments (12S-RNA, 16S-RNA, Cytochrome-b) that the osteological results were fundamentally correct, with a major exception. The Aplocheilus-Pachypanchax genera from Madagascar, Seychelles and Indo-Asia are shown to be basic to all Aplocheilids, with two descendants, one in Africa and one in South America, each producing all the extant, annual or non annual, species. A primary consequence of this result was not pursued by these authors: the extant presence of Aplocheilus-Pachypanchax, only in regions that drifted away before the continental divide, and of several externally primitive morphotypes in today Guinée, Nigeria, Tanzania and Colombia-Venezuela, Sertao do Brasil, Uruguay-Argentina (fig.2), implies that the entire pre-drift or early post-drift Gondwana -or at least all its coastal parts- could have been inhabited by tropical Cyprinodonts before the Tertiary (more than 90 MYA) or even since the early Cretaceous (135 MYA). However, because of the coastal origin of these extant morphotypes and because of the older versatility of tropical Cyprinodonts to marine environments, it seems unreasonable to speculate more precisely on these dates (see further, § 4.3.3).
Fig. 3. The relative position of Africa with respect to South America (120 MYA). The South Atlantic, south of the Niger delta has opened up by rifting that entered the Bénoué Trough. Africa, north of the Niger river, has remained fixed with respect to South America. The mesozoic Rift is also drawn as a putative paleo-migration route (Goldblatt, 1993).
The recent paleobiogeographical knowledge, outside Cyprinodonts, concurs with the molecular and the osteological evidences.
The present paleontological knowledge is much behind. The ancient basic morphotypes and their fossil relatives are associated with a minimum age (circa 30 MYA), much younger than the two major continental disconnections quoted above (90-135 MYA).
The purpose of this study is then to deepen comprehensively the parallel comparison undertaken for Rivulus and Aphyosemion. And to extend it to all Aplocheilids. It stands as a transversal analysis, and, as an evidence of the potentials of the basic ancestor to opportunistically respond to the variations in environment (similar situations-similar responses) and then… survive through its diversified descendants (distinctive responses). Its scope is also extended to the very different Aplocheilichthyins, which are the second group of (oviparous) Cyprinodonts inhabiting the tropical waters. Being better swimmers, they either live in different niches of the same biotopes or along edges of larger bodies of water, with also components in the Old and the New Worlds (with unfortunately a single group, Fluviphylax, in South America). It would have been interesting to add, to the analysis, the New World viviparous Poeciliins, which are the sister group of the Aplocheilichthyins, as ecological counterparts, but their knowledge is not available to the author.
The geographical scope of this study is then the tropical countries of Africa, America and Indo-Asia, where these two groups of Cyprinodonts are recorded (fig. 1, paleogeographic reconstruction of the two continents with the present countries local names). It excludes the temperate regions of these continents (e.g. the Mediterranean sector of Africa) or the very high mountains of tropical regions (e.g. the Andes).
The parallel comparison will be treated, for the sake of clarity, into independent topics:
1- The altitudinal and geological dimensions.
2- The past climatic variations and their impact on water mass.
3- The past climatic variations and their impact on terrestrial flora.
4- The local dimensions, the biodiversity and the ecology.
5- The behaviors, non sexual and sexual.
6- The morphotypes and the morphomeristics.
7- The color patterns and the genotypes.
Obviously these topics are fully interdependent. We shall attempt to avoid too many redundancies, by referring to other further or previous sections within the text.
On top of the point-to-point comparison, it appears primarily important to present one concept, one duality, one hypothesis that are federative to all Cyprinodonts, that are a key to their phylogeny and that need to be kept in mind all along the analysis.
* The superspecies concept.
* The sympatry-allopatry duality.
* The climatic-biogeographic hypothesis.
* The superspecies (or species-complex) represents a group of species which share a single direct common ancestor (a clade) and which show a strictly identical external profile. These very closely related, vicariant species are characterized by similar distribution schemes, by identical subniches preference, by similar shapes of body and fins, by sharing dominant micromorphological characters, by similar meristics and notably of the Dorsal/Anal relative deviation levels, by identical behavior, by the similar dominant choice of food (etc); they share key color pattern features and genetic mainframes, but are distinguished by details in them, inducing ethological (pre-mating) and sexual (post-mating) barriers. A superspecies, as a witness of recent explosive speciation of the Cyprinodonts, comprises many (three to over a dozen) presumably valid names. These are cryptic species (i.e. isomorphic and vicariant), although extremely rare, distinct and isolated, morphospecies have been attached to them, after DNA studies, as sister species to form a clade. A superspecies is rather easy to build up from living material in the field or in the aquarium. It is much more difficult to define with preserved only, especially old, material (Scheel, 1968; Huber, 1978, 1992, 1996).
* The sympatry-allopatry duality is the major force in populations dynamics of Cyprinodonts (sympatry is used in its restricted sense, also termed syntopy by some authors). This duality is enacted in two complementary rules (Huber, 1978). First, the isomorphic components of the same superspecies are strictly allopatric and they replace each other vicariantly. Second, the components of distinct superspecies are sympatric (obviously, if they occur in the same biological region). Females of each sympatric component will select the right male of her own species (and not the reverse) from characteristics of his color pattern, fin shape, behavior (etc.) (Brosset, 1982). Most frequently, two congeners of two distinct heteromorphic superspecies are sympatric, whereas it happens only occasionally and in restricted ranges for other groups of fishes (Huber, 1978, 1992). Even more, up to five species of distinct superspecies of the same ancestry have been reported sympatric, both in the today permanent (non annual fishes) and seasonal (annual fishes) biotopes, and seven if other Cyprinodont lineages are included (Huber, 1978, 1992, 1995).
* The paleoclimatic hypothesized relative stability and the geomorphological instability of the mid-late Tertiary after the continental drifts of the Mesozoic era, and, the paleoclimatic disorders and the relative geomorphological stability of the Quaternary are hypothesized here for the first time to be responsible for the evolutionary history of tropical Cyprinodonts. This is based on five key observations:
Then, this hypothesis induces two theoretical periods with two different types of events, even if many of these events were recurrent. The former, along the geomorphological events (earth uplifts, earth drifts, river reversals, epicontinental seas), with cumulative effects. The latter, along the climatic oscillations with sweeping effects (water maintenance in the generalized refugium). The former, for the basic morphotypes, progressively along the Cretaceous-mid Tertiary and then their somewhat derived morphotypes. The latter, for the explosion of cryptic species and of the genotypes from the then extant morphotypes, along the Pleistocene and early Holocene (at least, later than 2.5 MYA; probably also, even from as late as after the last glacial maximum, at 18000 BP- years before present). The former, for the migration patterns of large groups and subgroups. The latter, for the extension patterns of superspecies. However, the difference in time scale for these two theoretical periods must be stressed. The framework of the former is tens of millions years and may aggregate many heterogeneities and uncertainties (and major unknown extinction waves). The framework of the latter is thousands to a few millions of years and its history is being known with far more details.
These three federative characteristics are probably not shared (at least the first two) by most other groups of freshwater fishes. This is because, for ages, Cyprinodonts have been all, with variations, dwellers of rather reclusive biotopes, under cover, where they are dominant or even exclusive. They live in small shallow bodies of slow-moving or stagnant waters, often temporary or seasonal (non annual and annual Aplocheilids) or else in small or larger -but at their margins, only- rather moving waters (Aplocheilichthyins). So they tend not to encounter the group of populations that are neighboring them, each being compartmentalised a few kilometers apart. They are absent (or rare, even for the erroneously hypothesized riverine Fluviphylax) in the deep mid-waters of large rivers, where most fishes live. This is also because Cyprinodonts, much more the Aplocheilids than the Aplocheilichthyins, are poor swimmers. The result of these two related factors (reclusive biotopes and slower mobility) is that the modes of distribution, evolution, survival and migration (… ) have their specificities and are rather different from the standard groups of fishes. Some groups of fishes -in small numbers- do indeed live at some age or stage in the Cyprinodonts reclusive biotopes. This is by chance (e.g. an invasion from the nearby river after the floods) or by specialization (e.g. the predatory behavior against the adults Cyprinodonts or their offspring), since the majority of their counterparts are to be found in the standard biotopes. None to our knowledge truly competes with the Cyprinodonts, in either the Old or New World, in terms of space, population density, food. It is of utmost importance to emphasize the reclusive character of the tropical Cyprinodonts (which cannot escape from this constraint, like the temperate more sea-tolerant Cyprinodonts): unlike standard riverine fishes, their waters are the first to suffer disturbances, up to desiccation in case of an unusually long drying period. This has major implications in both the Old and New Worlds, and for both non annual and annuals groups, in terms of evolution, speciation and expansion patterns.
Finally, for the reader who is not a Cyprinodont specialist, let's recall a point of systematics and nomenclature for the concept of species (Huber, 1996). The diversity of phenotypes, or even, of the so important male live color patterns, is lower than the genetic diversity. This implies that the number of biological species surpasses by far the number of distinguishable phenotypes (see the suggested reasons, § 2 and 3, in the past climatic fluctuations). This has led to a practical species concept (Huber, 1996) which limits species naming to isolated populations with at least one stable distinguishing external character. Then a species-name (i.e. a taxon at the species level) often encompasses several biological species that cannot be distinguished by phenotype.
The major paleontological dates, associated with putative biogeographical events affecting tropical Cyprinodonts, are given in Table 1, as a vital lead in the present study.
In addition, also as a vital lead for the reader, the postulated superspecies are characterized, in Table 2, according to their primitive (plesiomorphic) or derived (apomorphic) external characters, separately for the Aplocheilids and for the Aplocheilichthyins. And their biogeography is comparatively associated, within a vicariance approach.
Both tables also contain information and data that are not found in the text and provide with a different and supplemental viewpoint.
Abbreviations of taxa at the generic level follow Huber (1996). Generic and subgeneric names are alternatively used for argumentation purposes, clearly without a systematic objective. It goes without saying that the precision "ancestor of" is mostly omitted when extant species are mentioned within an historical context. This is for simplicity sake. Country names are given with their local spelling. Sources are given in the bibliography, which is intentionally limited to general references.
This thorough detailed and parallel comparison of the characteristics of Old World and New World tropical Cyprinodonts is the first transversal and global analysis in this group.
Of course, the modern knowledges in tectonic plates and in palynology are better founded. They have permitted that this comparison is structured and argumented.
Even if still a lot has to be understood, deepened or simply confirmed by experiments.
Finally, we would like to synthesize the various aspects of this comparison with a different viewpoint and in two segments. The similar responses to the same changes, the different and apparently specific responses to these changes. The former may be reflecting the memory of the ancient Cyprinodont phenotype, the latter may be its first true differentiation between the three aggregate regions, after probable considerable extinction intervals.
Similar responses to similar changes or situations:
- The various potential niches are occupied similarly in Africa and America, either by annual or non annual Aplocheilids in reclusive passive waters or by Aplocheilichthyins in somewhat less reclusive active waters. It is a shame then that no annual component has been transferred into Asia along the northern drift of Madagascar and India.
- The general distribution pattern is clearly the same in all regions, with 5 possible longitudinal strates along the coast (marine, brackish, freshwater coastal lagoons, internal lowlands including the cuvettes, and the neighboring plateau). Within the plateau itself, vertical patches of superspecies are similarly observed. This major shared asset is all the more important that it is not seen, to our knowledge, in the other major groups of fishes, which are linked to river drainages. Apart from the key roles of the transition coastal plain-plateau and of the fluctuations of the sea level, the major driving force appears to be the forest coverage -or conversely, the ephemeral biotopes continuity- over past periods.
- The general response to disturbances is the same, whatever it stems from climatic fluctuations (here the key role of refugia can be exemplified) or from tectonic disruptions creating constraints and opportunities.
- The general speciation mode, by vicariance, is the same whatever the basic group is concerned: diversification of superspecies at borders with frontier species as a direct consequence of migration from relict places of the past dry maximums.
- The same local structure of independent micropopulations -of the same species or of sympatric distinctive superspecies- is a consequence of the defensive selection of reclusive biotopes and of the neutralist behavior, by these fishes, contrary to other groups of fishes.
- The global evolutionary response is the same in terms of general morphotype. The observed stability is associated with a detailed variability of morphomeristics and a highend diversity of color patterns and of genotype. The dwarf relict specialized species occur similarly in the three continents. The potentiality of the viviparity and of sex chromosomes is available in the Old and New Worlds.
- The general behavior in tribes or schools is the same, whatever the position in the continuum of annualism to non annualism.
Distinctive responses to similar changes or situations:
- The combination of derived characters is clearly not the same in the Old and the New Worlds. This concerns details of morphology (head shapes, fins shapes and extensions, the cylindrical or deep profile of body, frontal scalations, cephalic neuromast patterns, etc.), of color patterns (organization, specificities), of behavior (particularities, like aestivating). However, each specificity disclosed in one continent for one group also occurs in the other, less exacerbated.
Nobody will now contradict the fact that African, American and Indo-Asian Cyprinodont faunas are separated for so long -at least 90 million years- that resemblances are more the result of convergence than anything else. But these convergences occur everywhere among the two very homogeneous phylogenetic groups, the Aplocheilids and the Aplocheilichthyins. The resemblances are so numerous that the homoplastic characters, derived from a similar or a different response to similar situations, should be related to each of the two basic ancestors. And much less to a stochastic chance.
No doubt these fishes are in every way very different from the standard river fishes and opposite by major traits:
- independent micropopulations of sympatric congeners in reclusive fragile biotopes where they are quasi-exclusive;
- explosive recent genotypes and typified color patterns, together with an amazing basic morphological stability (only 5 basic morphotypes, 3 in Aplocheilids, 2 in Aplocheilichthyins);
- probable recurrent extinction episodes except in refugia, from where a brand new expansion process started again.
The important finding of this study is that, by combining data of paleogeography, paleoecology, vicariance, endemicity, diversity and external characters of extant phylogenetic lineages, it is possible to hypothesize their centers of origin as well as plausible scenarios of the long term history and migration patterns of tropical Cyprinodonts.
The main additional finding of this study is that, contrary to previous publications, the explosive evolution of the tropical Cyprinodonts, is to be found in the near past. Apart from the very old development of the few distinguished morphotypes linked to major Earth events, most of the evolution spur is hypothesized to be recent, linked to climatic fluctuations and especially to the late glacial maximums of the Pleistocene-Holocene. The evolution of these fishes, pushed by similar and severe constraints, is playing with a limited number of options. The many similarities between the Old and the New Worlds characteristics change then somewhat the picture from a purely haphazard convergence into the disclosure of very few options, variably combined as much as possible.
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