Goldschmidt (1940) defined macroevolution as evolution above the species level and envisaged speciation as the crossing of a threshold of major genomic reorganization. Although his specific ideas of change are now outmoded, the mechanisms and effects of speciation are still hotly debated, and many still see speciation as a vault through the looking glass, leaping past new evolutionary thresholds. The punctuated equilibrium hypothesis, for example, is in search of a mechanism that focuses most morphological change at the time of speciation. The crux of the matter is how to relate genetic and phenotypic variation within a population to divergence between species. Are spe-ciation and the subsequent genetic divergence merely an extrapolation of within-pop-ulation variation, or is there a consistent jump in genetic and phenotypic difference? If speciation is a special time of reorganization, then the elaboration of large phenotypic differences in evolution would be enhanced both by the rate of speciation and by extinction that is selective relative to a suite of morphologies. Macroevolutionary questions place a magnifying glass on our understanding of speciation and its effects.
Our discussion can best be framed as a series of questions:
1. What are species?
2. Are the genetic differences between species of the same sort as intraspecific differences?
3. Does speciation accelerate differences important in major evolutionary change? Indeed, is that what speciation is about?
4. If the differences are significant, then does this make a difference to theories concerning the process of macroevolution?
5. Are species accidents or adaptations?
A sketch of the history of species concepts should be kept in mind as we consider these questions. Species concepts break down into a few categories:
1. Typological species concept (Linnaean)
2. Biological species concept
3. Evolutionary species concept
4. Phylogenetic species concept
5. Recognition species concept
The original typological concept was essentialist; species were endowed with a platonic essence (see chapter 1). Practically speaking, philosophy does not matter, for many species can be distinguished by morphological differences, and there are examples of peoples able to nearly match the acumen of the most advanced system-atist (although sibling species can't be included in this). Therefore, it is no surprise that as the issue of essentialism disappeared in the twentieth century, systematists still took the species level to be fundamental. In its new guise, it became a morphological species concept, which defined species typologically by key identifying characters. Although variation was not ignored, identification and distinguishing features were the foci of species. If you named a new species, you had to (and still have to) deposit a series of types in a collection and recount why this form differed from all other named species.
It was only with the advent of such works as Haldane (1932a), Dobzhansky (1937), and Mayr (1942) that the Darwinian notion of species mutability and the neo-Darwinian theories of genetic change were united into a general theory that saw species as arising from within-species variation but bound by membership in a common reproductive community. Divergence between daughter species was thought to be of the same qualitative sort as geographic divergence within species. Separation led to fixation of genes that caused incompatibilities when isolated populations again came into contact, though species were believed also to be under selection after contact for prezygotic isolating mechanisms and ecological divergence from other species (Dobzhansky 1937, Mayr 1963). Of course, the multiplication of species allows for the multiplication of independent evolutionary units that can respond in different evolutionary directions.
Reproductive isolation is the cornerstone of the biological species concept. "Species are groups of actually or potentially interbreeding populations that are reproductively isolated from other groups" (Mayr 1942). Note that this concept cannot, of necessity, apply to asexual organisms. More importantly, there are likely many isolated species (at least under this definition) that are reproductively compatible but do not interbreed currently, even though they may be distinctly different morphologically and genetically. Thus, the biological species concept allows for three cases:
1. Complete geographic separation of two species
2. Geographic contiguity of the geographic ranges of the two species
3. Sympatric occurrence of two species, who do not interbreed
Many of the phenotypic differences between species may not have caused, nor contribute at present, to reproductive isolation. Indeed, there is no necessary scale of phenotypic difference that we can use to define a biological species, even though there are metrics of genetic distance and phenotypic difference that, on average, predict separation at the species level reasonably well. Because there are many instances of morphologically nearly indistinguishable sibling species, we can state with authority that morphological jumps in speciation fail to occur in many species complexes. We cannot, however, readily predict that speciation will generate a given amount of morphological divergence. For example, the Tropheus lineage of the cichlid radiation in Lake Tanganyika consists of a large group of species that are morphologically nearly identical but nevertheless quite genetically divergent (Sturmbauer and Meyer 1992). This lineage of six species contains twice as much genetic variation as the entire morphologically highly diverse cichlid assemblage of Lake Malawi.
One conflict underlies many of the current arguments in both speciation theory and population genetics. Species are regarded either as exquisite adaptations or accidents of divergence. The first alternative was championed by Dobzhansky (1937), who regarded speciation as a process involving intense selection for balanced and integrated gene pools, and, therefore, against pairings among individuals from different gene pools. Part of this adaptation was achieved when two formerly isolated populations were reunited. Selection against hybridization was part of the completion of the adaptations of the two new species. The selection resulted from hybrid inferiority in either of the habitats to which the daughter species had become adapted. The biological species concept became enmeshed in the issue of selection against hybrids, especially when considering sympatric sister species. This view of adaptation to local environments and against interbreeding contrasts with that of H. J. Muller (1939), who believed that after divergence, hybrid sterility arose by chance as a product of change in the genetic background, either by drift or adaptation to different biological situations. Isolated populations moved toward "ever more pronounced immiscibility as an inevitable consequence of non-mixing."
Evolutionary or anagenic species are temporal successions of fossil lineages that transform one into the next with no cladogenesis. They are used commonly by paleontologists (see chapter 6) and demonstrate that significant spans of geological time often witness a succession of transitions that involve a degree of morphological difference we encounter between extant and coexisting species. The definition must of necessity be phenotypic. On the one hand, one might argue that such changes do not involve splitting and therefore the entire lineage must be classified as a single species. On the other hand, the fact that so many evolutionary species have been established and continue to be recognized is a demonstration that phenotypic changes on the order of species differences can be achieved commonly without splitting. A slight variation of this definition allows cladogenesis. Here the environment is gradually shifting and a newly evolved descendant evolves and coexists with its ancestor for a time. Then as the environment continues to shift, the descendant supplants the ancestor. In the long run, this alternative leads to a similar anagenic chain of ancestors and descendants.
The phylogenetic species concept seems to derive nicely from the biological species concept, but it instead opens a can of worms. A phylogenetic species is an irreducible monophyletic cluster of organisms that is diagnosably distinct from other such clusters. Thus, each species can be mapped onto a cladogram. Phylogenetic species can be regarded as the smallest monophyletic group of common ancestry (deQueiroz and Donoghue 1990). This definition can be consistent with the biological species concept, but it eschews considerations of reproductive isolation. Although Mayr's definition, quoted above, does not necessarily require anything more than a lack of interbreeding, many additional aspects of the biological species concept (e.g., reinforcement of isolation by secondary contact) are absent from the phylogenetic species concept. Indeed, it is fair to say that proponents of the phylo-genetic species concept feel that cladistic status is the only means of recognizing species. Species, therefore, are recognized by synapomorphies.
The phylogenetic species concept has the advantage of consistency with evolutionary descent, but species concepts come into conflict over the issue of reproductive isolation. Consider a case in which a series of populations can be distinguished by characters, but one of the populations, the most derived, is reproductively isolated from the others (Figure 3.1). A cladistic consistency argument will immediately identify the members of species A as paraphyletic, even if derived species B is mono-phyletic.
This problem can be merely annoying, but things can be much worse. For one thing, phylogenetic species could readily consist of a group of populations that are currently, but ephemerally, identifiable as monophyletic groups. It may well be that all three populations of A (Figure 3.1) might introgress completely, leaving a simpler tree of A and B as terminal taxa. The phylogenetic systematics approach tends to reject such dispersal possibilities, which is probably why there is no great concern for such mixing.
As time passes, this problem will probably diminish. If stabilizing selection is very strong then alleles may be retained for long periods of time in two species that descend from a parent species. Otherwise, alleles will be lost by drift, so the probability of introgression of alleles by hybridization will decrease. In general these problems exist in the short run because trees of genes are not the same as trees of divergent taxa. The same alleles may be inherited by two daughter taxa that are
Figure 3.1. A cladogram showing population B, which is reproductively isolated from the three A populations. If the three A populations are reproductively compatible, then conflicts exist between the biological species concept and the phylogenetic species concept.
reproductively isolated, or each daughter may stochastically inherit different alleles. After a time, however, drift will result in alternative alleles being fixed in the different descendant taxa.
In the recognition species concept, species are the most inclusive population of individual biparental organisms that share a common fertilization system (McEvey 1993; Paterson 1985). Paterson believed that Mayr overemphasized isolating mechanisms between species. He argued that species arise as incidental consequences of adaptive evolution entailing individual selection, as opposed to species being "adaptations," having coadapted gene complexes that isolate them from other species. Isolating mechanisms would have an advantage in the zone of overlap between incipient species but not otherwise. The cohesive species concept (Templeton 1989) also argues for the importance of cohesive properties of species. This latter notion, however, is consistent with Dobzhansky's ideas of an integrated genotype, fashioned by natural selection, whose fitness would be lowered by cross-breeding with other closely related species.
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