What is phylogenetic species concept?

Define and apply the biological, morphological, ecological, and phylogenetic species concepts, while recognizing that speciation is a process.
Distinguish between sympatric and allopatric speciation.
Define, recognize, and understand the significance of reproductive isolating mechanisms in reducing gene flow between populations.
Distinguish between prezygotic and postzygotic barriers to reproduction.

Biologists have a long tradition of debating how to define a species. The most prominent and relevant definitions for us are framed around:

the ability of two individuals to successfully produce viable, fertile offspring (biological species concept)
whether individuals look similar (morphological species concept)
how closely related individuals are evolutionarily (phylogenetic species concept), and
whether the individual use or can use the same set of biological resources; in other words, whether they occupy the same “niche” (ecological species concept).

Which species concept is most useful depends on circumstance and available data. For instance, in the figure below, branches that don’t reach the top of the diagram represent extinct species (or taxa). Mastodons are no longer living, so it becomes impossible to know if mastodons from different populations were able to interbreed (biological species concept). We can look at their morphologies by comparing teeth, bones, tracks, and sometimes fur, and that gives us a basic idea of whether mastodons were of the same species (morphological species concept), but we don’t have lots of complete fossils to examine. We are left with a combination of fossil and DNA evidence that allows us to construct a phylogeny, which shows us that the combination of factors (fossil morphology, DNA comparison, geographic location) can be combined using an mathematical algorithm that groups species based on phylogeny (phylogenetic species concept). The morphological and phylogenetic species concepts are also more useful for analyzing asexually-reproducing organisms, such as bacteria, where the biological species concept isn’t relevant at all since there is no interbreeding! The ecological species concept is useful for analyzing cases where individuals in a lab or zoo environment might be physically capable of interbreeding, but would never actually encounter each other in the wild because they occupy different ecological niches. We’ll review an interesting example of this in class.

The only illustration in Darwin’s On the Origin of Species is (a) a diagram showing speciation events leading to biological diversity. The diagram shows similarities to phylogenetic charts that are drawn today to illustrate the relationships of species. (b) Modern elephants evolved from the Palaeomastodon, a species that lived in Egypt 35–50 million years ago. (Source: OpenStax Biology)

Here is a short, fun video contrasting the morphological and biological species concepts:

Speciation is a Process

Speciation, or the process that results in new species, occurs when an ancestral population splits into two or more descendant species which are genetically distinct and unable to interbreed (per the biological species concept). Speciation is all about gene flow—or lack thereof. The less gene flow, the more likely speciation is to occur. There are two different mechanisms of speciation, based on the mechanism that prevents gene flow: allopatric speciation and sympatric speciation.

Allopatric speciation can occur when two populations are physically isolated from each other (allopatry), creating the absence of gene flow. In the figure below, geographic isolation occurs when a beetle population is divided by a body of water that prevents interbreeding between the two populations. Small changes occur in each isolated population over time, and if changes occur that prevent successful production of fertile offspring, then when the isolating ‘barrier’ is removed, the two populations can no longer interbreed.

What was once a continuous population is divided into two or more smaller populations. This can occur when rivers change course, mountains rise, continents drift, or organisms migrate. The geographic barrier isn’t necessarily a physical barrier that separates two or more groups of organisms — it might just be unfavorable habitat between the two populations that keeps them from mating with one another (University of California Museum of Paleontology’s Understanding Evolution (http://evolution.berkeley.edu)

Sympatric speciation occurs when two populations in the same location become unable to interbreed due to reproductive isolation, which reduces gene flow between populations and thus increases the likelihood of speciation occurring. Reproductive isolating mechanisms can be pre-zygotic or post-zygotic, which is a jargon-rich way to say before or after sperm and egg unite to form a zygote. Pre-zygotic reproductive isolation can include:

behavioral differences in mating song or dance, meaning individuals don’t even recognize each other as possible mates
differences in when and where individuals attempt to mate, meaning that individuals don’t ever encounter each other for mating
or sperm-egg incompatibility, meaning that individuals might attempt to mate, but it is not possible for the sperm to fertilize the egg.

Post-zygotic reproductive isolation can include:

developmental failures and spontaneous abortion, meaning that the embryo does not develop properly and is therefore inviable (not capable of living)
growth and development of a viable (living) fully formed adult offspring that are themselves sterile (infertile), meaning that the offspring are not capable of reproducing.

Watch this Crash Course Biology video for a 10 minute overview of speciation that hits all the salient points.

Evolution of pre-zygotic reproductive isolation mechanisms

When interbreeding occurs between two different species (or two different populations in the process of becoming different species), the resulting offspring is called a “hybrid.” In biological terms, a hybrid simply mean something from two different sources; in this case, two different species. One interesting question is how pre-zygotic isolation mechanisms can evolve during sympatric speciation. As with all evolution by natural selection, the key element to focus on is biological fitness. If the hybrid offspring is less biologically fit (has lower reproductive success) than the non-hybrid offspring (offspring that result from within-population mating), then that means the parents of the hybrid offspring had traits that lowered their fitness because of their mating with an individual from the other population. As a result, any trait that reduces cross-population interbreeding will be selected for in those two different populations, and any trait that promotes cross-population interbreeding will be selected against in those two different populations. In other words, pre-zygotic barriers to reproduction are adaptations that reduce the likelihood of inter-species breeding, and they arise when the hybrid offspring have low biological fitness.

A new population that results from a speciation event is called a species. But although species result from a simple process, recognizing species in nature can be complicated. Biologists cannot travel in time to observe the speciations that resulted in today's diversity of life, so they must observe the reproduction of living organisms to determine the makeup of species. Paleontologists can find the fossil evidence of the ancestors of today's species, but they cannot observe whether those fossil organisms could reproduce with each other. Because scientists have different kinds of evidence about organisms, they use different concepts of species when testing hypotheses about their evolution.

Biological species

The most obvious property that helps to define species is reproductive isolation. Biologists studying living animals often use the biological species concept, which envisions a species as a "group of actually or potentially interbreeding natural populations which are reproductively isolated from other such groups" (Mayr 1942). It is the biological species concept that primatologists use to grapple with whether chimpanzees and bonobos are different species, for example, by observing the differences in their reproductive behaviors and the strength of geographic isolation between their populations.

The biological species concept has some important limitations for paleontology. Making use of the concept depends on observing the mating behavior and interbreeding patterns of animals in their natural environments, which is not possible with fossils of organisms that lived in the past. Other kinds of observations that paleontologists might gather, such as morphological differences between fossils, have no necessary value under this concept. Another limitation is that the biological species concept does not incorporate any idea of how species may change over time. Paleontologists study fossils that may be separated by hundreds of thousands of years of time. It is difficult to imagine such widely separated individuals as part of the same reproductive community, even if they were very similar to each other. Over such time periods, evolution can transform populations substantially. The biological species concept recognizes the genetic continuity within a species caused by gene flow, but it does not incorporate a view of species existing over evolutionary time. For these reasons, paleontology requires a different kind of species concept.

Phylogenetic species concept

The phylogenetic species concept is an attempt to define species by their relationships to other species. Instead of trying to determine the reproductive boundaries of populations, scientists using the phylogenetic species concept attempt to uncover their genealogical relationships. A group of individuals that includes all the descendants of one common ancestor, leaving no descendants out, is called a monophyletic group.

Paleontologists Niles Eldredge and Joel Cracraft devised a species concept called the "Phylogenetic Species Concept," intended to apply to circumstances in which reproduction or isolation among organisms could not be observed. Under this concept, a species is "a diagnosable cluster of individuals within which there is a parental pattern of ancestry and escent, beyond which there is not, and which exhibits a pattern of phylogenetic ancestry and descent among units of like kind" (Eldredge and Cracraft 1980:92).

Key to the phylogenetic species concept is the idea that species must be "diagnosable." In other words, members of the species should share a combination of characteristics that other species lack. To look for the unique features that define a phylogenetic species, paleontologists must perform systematic comparisons with other related fossils or living species. These aspects of the concept make it widely applicable in paleontology.

But the phylogenetic species concept is not without its problems. Because the concept defines species based on morphology, without explicitly referring to populations or reproductive boundaries, it does not apply well to cases where morphologically different populations are connected by gene flow. Morphological variation among populations is not uncommon within living species. Humans today are a species with substantial morphological variation from continent to continent. Humans on different continents are not reproductively isolated, and their variation is largely distributed as clines over large geographic distances. Yet a paleontologist who had only a few fragmentary specimens from each continent would not necessarily know the pattern of variation, and many features of his specimens would appear to be unique. What would the paleontologist make of the high nose of a European specimen, the forward-facing cheeks of an Asian fossil, or the strong browridge above the eye orbits of an Australian, each taken randomly from their variable populations? By applying the phylogenetic species concept, a paleontologist would probably conclude that the different continents were homes to different human species.

Thus, because the phylogenetic species concept does not identify species based on the reproductive boundaries between them, it may have the effect of identifying populations connected by gene flow as different species. For this reason, a phylogenetic species as defined by a paleontologist may not correspond to a real prehistoric population that was the product of a speciation. Some paleontologists do not view this potential conflict as a problem, because identifying species based on unique characteristics will create as full as possible a systematization of the evolution of new features. Assuming that the number of ancient species was very large, and the number of fossils representing each of them is very small, then paleontologists can hardly hope to identify every speciation event in the past. The phylogenetic species concept may therefore provide a better approximation of the number and diversity of species that existed than other alternatives.

On the other hand, identifying populations connected by gene flow as different species can be a significant problem for paleontologists who take a greater interest in the processes of evolution than in the diversity of species in the past. Gene flow is a significant force shaping evolutionary change within populations. Moreover, evolution may cause a single species to change over time, possibly acquiring new unique features without any division of a species into separate reproductively isolated populations. Some paleontologists approach these difficulties by altering their view of the evolutionary process. If speciations can happen as a transformation of a single population in addition to the appearance of reproductive boundaries between populations, then a single evolving population may over time comprise several phylogenetic species. Or if most evolutionary change happened at the time of speciation, as asserted by the concept of punctuated equilibrium, then the phylogenetic species concept might more closely approximate the actual pattern of speciations in the past. But without such assumptions, the phylogenetic species concept's problems sometimes create a stumbling block for some paleontologists in attempting to understand the evolutionary process.

Evolutionary species

The evolutionary species concept combines the genealogical basis of the phylogenetic species concept with the genetic basis of the biological species concept. An evolutionary species is a lineage of interbreeding organisms, reproductively isolated from other lineages, that has a beginning, an end, and a distinct evolutionary trajectory (Wiley 1978). The beginning of a species' existence is a speciation, as a population becomes reproductively isolated from a parent population. The end of a species occurs either with extinction or with the branching of the species into one or more descendants.

Central to the evolutionary species concept is the idea of an evolutionary trajectory. The trajectory of a species is the evolutionary pattern of its characteristics over time. For example, one of the earliest species in the story of human evolution, Australopithecus afarensis, is represented by dozens of fossil teeth and mandibles, as well as other remains. Paleontologists hypothesize that these fossils, from several sites in East Africa, are members of a single species because of their many morphological resemblances. No very similar fossils have ever been found before 3.6 million or after 3 million years ago, dates that appear to indicate the beginning and the end of the species.

Nevertheless, the fossils do show some differences that appear over time. Although the molar teeth of the fossils do not change over time, the mandibles are thicker and more massive in more recent fossils than in the most ancient ones. As far as paleontologists can test, the mandibles form a single series evolving over time toward greater size and thickness. The evolutionary species concept infers that the fossils represent a species, beginning 3.6 million years ago and ending 3 million years ago, with an evolutionary trajectory that includes the evolution of greater mandibular thickness, without apparent changes in molar sizes.

The strength of the evolutionary species concept is that it allows paleontologists to focus on the causes of evolutionary change, whether they occur during speciations or at other times. Regarding A. afarensis, the observation that mandibles increased in size during the existence of the species may be explained by different evolutionary forces and conditions than if all the change occurred with the reproductive isolation of a new population. Although the greater mandibular thickness of later mandibles might be a unique feature, attempting to establish a new phylogenetic species for the later fossils might detract from an explanation of the overall evolutionary pattern.

Phylogenetic species vs. evolutionary species concepts

<br /> But the evolutionary species concept also has its problems. Because it uses several different criteria, much more information may be necessary to define an evolutionary species. Some scientists do not view this as a drawback, since even if a scientific view of the species that once existed and their boundaries and relationships proves a challenge, it may nevertheless add to our understanding of the evolutionary process.

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Yet for many paleontologists, the need to amass great numbers of fossils from different times makes the evolutionary species concept nearly impossible to implement. At the same time, if scientists always hold out the possibility that two different fossils were actually connected by gene flow, it may impede an understanding of evolutionary changes that accompany the appearance of new reproductively isolated species. If we want to have a scientific, meaning falsificationist, view of the species that have existed and their boundaries and relationships to each other, we must accept that the process will in many cases be difficult. Simply making up many species hypotheses cannot add to our knowledgeand in many cases it may detract. What is important is that we realize that our record of past species is incomplete, and our failure to substantiate the existence of many species in the past does not constitute evidence that they did not exist.

Testing species hypotheses

However species are defined, whenever scientists identify a species, they actually are stating a hypothesis about the relationships among individual organisms. Such a hypothesis may be tested using morphological, genetic, or behavioral evidence. Discovering real species that existed in the past involves predicting the morphological variability of populations, including variation that occurs among populations connected by gene flow. In the relatively small fossil samples available to paleontologists, determining the number of species in a sample is a significant problem. Researchers use a number of techniques to test species hypotheses with limited morphological samples.

Two fossil hominids: different species or not?

What is the level of morphological difference between two or more specimens? Using a living species for comparison, scientists can determine the likelihood of sampling similar variability as the fossil sample (Miller 2000).
What are the relative frequencies of characteristics in two samples of fossils? Statistical comparison with the differences between different populations within a living species can determine whether the differences in frequencies observed in the fossils would be likely to occur within the comparison species. Such comparisons can be extended to the differences between the sexes of a living species to test whether sexual dimorphism accounts for differences between fossils (Lee 1999).
How do morphological features covary? If one fossil sample has a high incidence of several features that are absent or at low frequency in another sample, this supports the hypothesis that the two samples represent different species. With samples of sufficient size, say, 10 individuals or more, paleontologists can even estimate the maximum level of gene flow consistent with the morphological differences, and thereby frame a test of the hypothesis of different species in solid evolutionary terms (Hawks and Wolpoff 2001).
Do samples represent change over time? Sometimes paleontologists can use different populations from living species to evaluate likelihood that certain kinds of changes might occur over time. The best comparisons are with large samples of fossils that represent long spans of time, however. Although the evolutionary process is in ways unique for each species, analyses of the rate and level of changes in other species provide the most powerful tests of species hypotheses available in studying the past.

References:

Eldredge N, Cracraft J. 1980. Phylogenetic patterns and the evolutionary process: Method and theory in comparative biology. New York: Columbia University Press.

Hawks J, Wolpoff MH. 2001. The accretion model of Neandertal evolution. Evolution 55:1474-1485. PubMed

Lee SH. 1999. Evolution of human sexual dimorphism: Using assigned resampling method to estimate sexual dimorphism when individual sex is unknown. Ph.D. thesis, University of Michigan.

Mayr E. 1942. Systematics and the origin of species from the viewpoint of a zoologist. New York: Columbia University Press.

Miller JMA. 2000. Craniofacial variation in Homo habilis: An analysis of the evidence for multiple species. Am J Phys Anthropol 112:103-128. PubMed

Wiley EO. 1978. The evolutionary species concept reconsidered. Syst Zool 27:17-26.