Cadernos Lab. Xeolóxico de Laxe ISSN: 0213-4497 Coruña. 2001. Vol. 26, pp. 349-358

The problem of the concept in the phylogeny of the cave bears El problema del concepto de especie en la filogenia del Oso de las Cavernas

VILA TABOADA, M. & GRANDAL d’ANGLADE, A.

AB S T R A C T

This a short review of a series of concepts daily used in palaentology, trying to connect them with their meaning in other fields of study in Biology. Firstly, it should be pointed out if the concept of species comes from an empiric reality or if it has arisen from the scientific need of assembling. The evolutive concept of , as well as its "methods" seem to be based in the term population. Hence, as meaningful discussions on speciation require a common definition of its end result, namely species, a solution to the tricky issue of defining species probably lies in a deeper knowledge of the processes behind speciation itself.

Key words: species, species concept, chronospecies, cave bear phylogeny Instituto Universitario de Xeoloxía Isidro Parga Pondal. Facultade de Ciencias. Campus da Zapateira s/n. University of A Coruña. E-15071. A Coruña. Galicia. Spain. ([email protected]) 350 VILA TABOADA & GRANDAL d’ANGLADE CAD. LAB. XEOL. LAXE 26 (2001)

INTRODUCTION of generation, produce other forms, but always similar to themselves: thus, there It is well know the complexity of usual are as many forms as number of structures phylogenetic disussions in living groups before present. such as Ursidae (panda, polar bear...). But, The Linnaean species concept was that when taxa are involved, the problem species were static entities of fixed charac- remains in the very concept of species. teristics which defined them as being part It should be wondered whether the of a group. He did not explicitly define concept of species comes from an empiric "species". Indeed, there is some conflation reality or if it has arisen from the scienti- between the Linnaean category "genus" fic need of sorting out organisms. The and what we consider a "species" or a spe- evolutive concept of speciation, as well as cies today. its "methods" seem to be based in the term population. Hence, as meaningful discus- sions on speciation require a common Lamarck (1802) definition of its end result, namely spe- Species is every collection of similar cies, a solution to the tricky issue of defi- individuals which the process of genera- ning species probably lies in a deeper kno- tion perpetuates within the same stage. wledge of the processes behind speciation Thus, the circumstances of their situation itself (ÖDEEN 1996). do not change enough as to vary their cos- tumes, habits or form.

HISTORICAL OF THE Darwin (1859) SPECIES CONCEPT It s absolutely undefined the number of differences considered as necessary in Aristotle (384-322 BC) order to give the category of "species" to two forms (...) I just consider the species An animal, an individual, cannot be concept as something arbitrarely used for eternal, because the reality of every being a group of individuals with strong simila- is found in its characters... which is speci- rities, but this concept do not differ of the fic (eidei). And thus, it always exists a variety term which is given to less diffe- genus (génos) for humans, for animals, for rent and variable forms. plants. Ernst Mayr (1942) Linneaus (1751) Species are groups of actually (or There are many species which the potentially) interbreeding natural popula- Supreme Being has created with a lot of tions which are reproductively isolated different forms. They, following the laws from other such groups. CAD. LAB. XEOL. LAXE 26 (2001) The problem of the species concept 351

Theodosius Dobzhansky (1935). and-fast definition, for since most evolu- Dynamic nature of the species con- tion is a gradual process, borderline cases cept must occur. And in the second place, we must not expect a single or a simple basis Species is a stage of evolutionary pro- for definition, since species arise in many cess at which the once actually or poten- different ways. tially interbreeding array of forms beco- mes segregated in two or more separate arrays which are physiologically incapable Smith (1994) of interbreeding. Species are distinguished on phenetic differences, be they morphological, Huxley (1942) physiological , biochemical, or genetic. All characters that very among the speci- In general, it is becoming clear that we mens under study are scored and a taxon- must use a combination of several criteria character matrix constructed. This matrix in defining species. Some of these are of is the subjected to multivariate analysis in limiting nature. For instance, infertility order to identify discrete clusters of indi- between groups of obviously distinct viduals based on total morphological mean type is a proof that they are distinct variation. The smallest clusters recognisa- species, although once more the converse ble then are a species. is not true. Thus, in most cases, a group can be distinguished as a species on the basis of the following points: DIFFERENCES AMONG THE 1.- a geographical are consonant with a CURRENT SPECIES CONCEPTS single origin 2.- a certain degree of constant mor- phological and presumedly genetic diffe- Biologic rence from related groups The Biologic Species Concept (BSC) 3.- absence of intergradation with rela- has undergone a number of changes over ted groups the years. Du Rietz defined it (1930) as: In most cases a species can thus be the smallest natural populations permanently regarded as a geographically definable separated from each other by a distinct discon - group, whose members actually interbre- tinuity in the series of biotypes. Barriers to ed or are potentially capable of interbree- interbreeding are implicit in this defini- ding in nature, which normally in nature tion. Some years later, Dobzhansky defi- does not interbreed freely or with full fer- ned a species as we have seen above, but tility with related groups, and is distin- later (1951) he relaxed this definition to guished from them by constant morpholo- the point that is substantially agreed with gical differences. Thus, we must not Mayr’s (1942), which is the accepted BSC. expect too much of the term species. In Strengths: fits within population gene- the first place, we must not expect a hard- tics. Gives an unambiguous empirical cri- 352 VILA TABOADA & GRANDAL d’ANGLADE CAD. LAB. XEOL. LAXE 26 (2001) teria. It provides an important conceptual Complements the biological species framework for speciation concept Weaknesses: Only really applicable to Mate recognition can be more easily the present (paleobiological work on evo- determined than ability to breed (espe- lution cannot use this concept). Doesn’t cially in non-living species) apply to asexual organisms (it is less use- We a k n e s s e s: Isolation mechanisms, ful in botany). No evolutionary dimension which lead to speciation are more difficult to conceptualise. No evolutionary dimen- Phenetic sion

Cronquist (1988) proposed an alterna- Ecological tive to the BSC that he called a renewed practical species definition: "the smallest Strengths: it corresponds to the fin- groups that are consistently and persis- dings of a considerable body of ecological tently distinct and distinguishable by research which suggests that species ordinary means". occupy "adaptative" zones which are deter- Strengths: is in fact the way we recog- mined and reinforced by the resources nize species differences. Works well for exploited an the habitats occupied sexual and asexual organisms. Applies Weaknesses: Is only loosely connected well to past species. to genetics Is rigidly tied to ecological Weaknesses: does not connect with niches determining species (consider that genetics. even in different life stages an organism Comments: the requirement that spe- will occupy different niches). Perhaps the cies be persistently distinct implies a cer- best that can be said is that ecological pro- tain degree of reproductive continuity. cesses influence phenetic and genetic This is because phenetic discontinuity aspects of species. Has no evolutionary between groups cannot persist in the dimension. absence of a barrier to interbreeding. This definition places a heavy, though not Cladistic/Phylogenetic exclusive, emphasis on morphological characters. It also recognizes phenetic cha- There are several definitions. All of racters such as chromosome number, chro- them assert that classifications should mosome morphology, cell ultrastructure, reflect the best supported hypotheses of secondary metabolites, habitats and other the phylogeny of the organisms. There are features. two types of phylogenetic species con- cepts: Recognition 1.- A species is the smallest cluster of organisms that possesses at least one diag- S t r e n g t h s: Fits within population nostic character. This character may be genetics (it is based on reproduction). morphological, biochemical or molecular and must be fixed in reproductively cohe- CAD. LAB. XEOL. LAXE 26 (2001) The problem of the species concept 353 sive units. it is important to realise that to explain evolution on all taxonomic this reproductive continuity is not used in levels. But to "pluralists" like S.J. Gould the same way as in the BSC. Phylogenetic crossing the level of species requires the species may be reproductive communities. postulate of a different process: macroevo- Reproductively compatible individuals lution. Macroevolution, as Gould sees it, need not have the diagnostic character of a is signified by large and sudden change, species. In this case, the individual need greater than what would be expected from not be conspecific. allopatric divergence alone (Ö D E E N, 2.- A species must be monophyletic 1996) and share on or more derived character. It should be reminded, no matter the There are two meanings to monophyletic: mode of speciation, the four forces which the first defines monophyletic group as all lead evolution: m u t a t i o n, m i g r a t i o n, the descendants of a common ancestor and selection and genetic drift. All of them, the ancestor. The second defines a are finally reduced or constraint by the monophyletic group as a group of orga- first one: mutation, its different rates and nisms that are more closely related to each its relationship with the other. other than to any other organism. Mechanisms that prevent gene exchan- Strengths: A clear evolutionary dimen- ge have been broadly termed i s o l a t i n g sion. Establishing phylogenies and, hence mechanisms. Some authors include in this branching points uses micro (e.g. DNA) category all factors that prevent gene and macro characteristics. It is the richest exchange, even geographical and spatial concept in palaeontological studies. isolation. Such geographically separated, Weaknesses: Only a very small number or allopatric, populations, obviously do of lineages have been uncovered given the not have the opportunity for gene exchan- detail required for this approach. ge, and it has been debated whether, given Disconnected from population genetics the opportunity, many of them would remain reproductively isolated. Another SPECIATION PROCESS question related to allopatry is the specia- tion due to founder effect (originated from Speciation is a special case in the evo- only a few coloniser individuals) and bot - lution of biological diversity. tleneck (group which has been substantially Traditionally, we know evolution as the diminished in size). Other authors have process where new forms of life are shaped therefore proposed that the term isolating through selective screening of biological mechanisms be restricted to those that variation, is this a real concept ? How does prevent gene exchange among populations speciation modify taxa ? Is it done by in the same geographic locality, that is, small, almost unnoticeable steps, ofter mechanisms that isolate sympatric popu- caller "missing links", as envisioned by lations. The latter have been classified by gradualists ? or is evolution less gradualis- Mayr into two categories: i) before fertili- tic ? To the modern synthesis it is natural zation (premating), as seasonal or habitat to extrapolate microevolutionary change isolation, behavioural or sexual isolation 354 VILA TABOADA & GRANDAL d’ANGLADE CAD. LAB. XEOL. LAXE 26 (2001) and mechanical isolation. ii) after fertiliza- Evolutionary changes may occur in tion (p o s t m a t i n g) as gametic mortality, species even if a speciation event (split) zygotic mortality or inviability does not occur. This kind of categorization and hybrid sterility (STRICKBERGER, results in naming chronospecies. Unlike 1990). biological species, chronospecies are arbi- The rate at which new taxa form is dif- trary divisions of a single evolutionary ficult to determine, as evolutionary rates lineage, defined on the basis of morpholo- differ even within phylogenetic groups. gical change (figure 2). These inconsistencies probably relate to Although the criteria used to delimit variations in selection pressures on the chronospecies boundaries are not descri- population at different times. Whether or bed in his formal definition, Simpson sug- not microevolutionary forces inducing gests that morphologic differences betwe- change within species are identical to en species should be at least as large as macroevolutionary forces generating new those between living species of the same species is a matter of contention taxonomic group. In our example, those (STRICKBERGER, 1990). differences should be similar to these found between the living representants of , URSIDS AND FOSSIL the genus Ursus (U. arctos, U. americanus, URSIDS U. maritimus...) But what are, in the cave bears, these For the , the presence of morphological differences? Sometimes the the time dimension makes it impossible difference between U. deningeri and U. spe - to apply the commonly accepted biologi- laeus is defined by the variation of some cal species concept. Thus, the continuous features, like the progressive Evolutionary Species Concept (ESC) was reinforcement and doming of the skull defined by Simpson as "a single lineage of and the jaw, or discrete ones, like the loss a n c e s t o r-descendant populations which of the three anterior upper and lower pre- maintains its identity from other such molars. lineages and which has its own evolutio- Continuous features are often difficult nary tendencies and historical fate" to be used as taxonomic character. The (SIMPSON, 1961). variability of size and morphology is a As fossil material carries the dimension constant in U. spelaeus and U. deningeri, of time, it often shows sequences of species even into the same population. This that are obviously related to one another, intraspecific variability is increased due to that follow one another in time, and are sex dimorphism or the existence of dwarf generally interpreted as evolutionary line- forms, like in high alpine populations. ages. Thus, according KURTÉN (figure Moreover, some sites from the Middle 1) it is no doubt that Ursus savini-Ursus Pleistocene show intermediate forms betwe- deningeri-Ursus spelaeus form a sequence of en both species, whatever it means evolutionary descent as well as a sequence (A LT U N A, 1972; RABEDER & of related species in time. CAD. LAB. XEOL. LAXE 26 (2001) The problem of the species concept 355

Figure 1. Phylogeny of Ursids. Adapted from KURTÉN (1976). There is a clear difference betwe- en U. deningeri and U. spelaeus.

Figure 2. Rapid and large morphological chan- ges in a single evolving lineage may lead to define different species (a and b) in successive geological intervals, wich are called chronospe- cies. The boundary between a and b is often subjective, but in any case it should be well defined. 356 VILA TABOADA & GRANDAL d’ANGLADE CAD. LAB. XEOL. LAXE 26 (2001)

Figure 3. Phylogeny of Ursids. Adapted from MAZZA & RUSTIONI (1994). U. deningeri and U. spelaeus are considered as a same group.

T S O U K A L A, 1990; A R G A N T, 1991, those based on a large number of samples. AUGUSTE, 1992). There is a lack of such studies that should The discrete features could be more be solved. But, despite of many paleonto- conclusive. But the study of the jaws of logists still consider both bears as separa- the Savini’s bear from Bacton reveals the ted species, there are other well documen- lack of the first, second and third premo- ted papers on Ursidae phylogeny that con- lar as a general feature. And concerning U. sider both bears as the same "group", i.e., deningeri, even some Mosbach’s skulls and the same species (MAZZA & RUSTIONI, jaws present a long diastema with no ante- 1994) as is shown in figure 3. rior premolars. These ones are seldom pre- Taking into account the definition of sent and, when present, the percent varies chronospecies, it is clear that only the from one population to another. morphological differences between two There is no doubt that the only reliable groups from a single lineage are conclu- studies on Cave Bear phylogeny would be ding for establish two different species. CAD. LAB. XEOL. LAXE 26 (2001) The problem of the species concept 357

The stratigraphic position of the bone basis, it is not possible, at present time, to remains gives not enough evidence to afirm that U. spelaeus and U. deningeri are make a separation. Moreover, the morpho- different species. Even KURTÉN (1976) logical change must be cuantified. In this left room for some doubt on this issue. 358 VILA TABOADA & GRANDAL d’ANGLADE CAD. LAB. XEOL. LAXE 26 (2001)

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