I.  Introduction

    A.  We have seen that there are two phenomena that (micro)evolutionary theory must explain in order to account for
          the diversity of life on earth:

        1.  Phyletic change within an evolving lineage

        2.  Splitting of lineages

    B.  Up until this point we have been talking exclusively about processes responsible for the former phenomenon.  Today,
          we shall considering the latter.

II.  Species and Speciation

    A.  The question of how a single evolving lineage splits into two independently evolving lineages (species) hinges on what
          we mean by "independently" evolving.

    B.  Intuitively, we might think that two populations are evolving independently if evolutionary change in one population
         does not influence evolutionary change in the other.

        1.  Another way of saying this would be that changes in gene frequencies in one population do not influence changes
             in gene frequencies in the other population.

        2.  But this can be true only if the populations are not exchanging genes; for if they are exchanging genes, then, say, an
             increase in the frequency of a particular allele in population A will bring about an increase in the frequency of that
             allele in the migrants moving between population A and population B, which in turn will cause at least a slight increase
             in the frequency of that allele in population B.

        3.  Thus, two lineages can be evolving independently only if they do not exchange genetic material.

        4.  Two phenomena may prevent genetic exchange between populations

            a.  There may be a physical barrier preventing migration between populations, and hence gene exchange.
            b.  There may be biological barriers, also known as isolating mechanisms, to gene exchange between individuals of
                 two populations.

        5.  There is a fundamental difference between these two phenomena: physical barriers are usually not permanent,
             whereas biological barriers to gene exchange tend to be.

        6.  Because physical barriers may break down, two daughter lineages arising from a single ancestral lineage, as long
             as they both persist long enough, will come back together when the physical barrier disappears.

        7.  Although the two populations may have diverged genetically during the time the barrier is in place, if there are no
             biological barriers to interbreeding when the physical barrier breaks down, individuals of the two populations will
             mate and coalesce back into a single lineage.

        8.  Achieving a permanent increase in lineage number after lineage splitting thus necessitates the evolution of biological
             barriers to interbreeding between populations.

        9.  It is for this reason that so much emphasis has been placed by biologists on the ability to interbreed as part of the
             definition of species, though we shall not be concerned with the debate over the appropriate criterion for distinguishing
             species.

        10.  Instead, we shall focus on understanding the mechanisms that lead to the evolution of biological barriers to gene
               exchange between populations.

    C.  Ecological barriers to coexistence

        1.  Understanding how biological barriers to gene exchange evolve helps us understand how the number of lineages
             present at any one time on earth can increase, and thus helps explain the generation of biological diversity.

        2.  However, it does not completely explain the spatial organization of the world's biological diversity.

        3.  In particular, while it explains the generation of related independently evolving populations, it does not guarantee the
             joint persistence of closely related lineages in the same area, i.e. it does not explain the many examples of closely
             related species coexisting.

        4.  As we shall see, a generalization known as Gause's Principle says that such coexistence requires that populations
             diverge in some important aspect of their ecology to allow coexistence, i.e that they exhibit character displacement.

    D.  The goal of this section of the course is thus to understand the evolutionary mechanisms that lead to the evolution of
          isolating mechanisms and to character displacement.
 

III.  Isolating mechanisms are of two types

    A.  Premating isolating mechanisms

        1.  Prevent individuals from different lineages from exchanging gametes when they encounter each other.

            a.  Behavioral mechanisms: e.g. differences in courtship displays, so that individuals of different lineages do not
                 recognize each other as potential mates.
            b.  Physiological mechanisms: e.g. differences in the seasonal timing of reproductive readiness, so that individuals of
                 one lineage are not reproductively active at the same time as individuals of the other lineage

    B.  Post-mating isolating mechanisms

        1.  Prevent offspring of crosses between individuals of different lineages from being either viable or fertile or both.

            a.  Examples
                --hybrid inviability: early embryonic death of hybrid offspring
                --hybrid sterility: failure of hybrids to produce functional gametes

IV.  Evolution of isolating mechanisms: the classical allopatric model

    A.  Objective: explain the evolution of both pre- and post-zygotic isolating mechanisms

    B.  Outline of the process

        1.  Originally, a single evolving lineage occupies some well-defined geographic area.

        2.  At some point, the lineage becomes divided into two or more distinct populations by a physical barrier.

            a.  Barrier may arise de novo within the original geographic range of the lineage (e.g. an uplifted mountain range,
                 a recently formed inland sea, a desert formed by recent climatic changes, etc.), or
            b.  Barrier may already exist, with the lineage on one side of it, and an unusual event allows migrants to cross the
                 barrier to form a new, peripheral, population physically isolated from the original population by the barrier.
            c.  In either case, the important characteristic of the barrier is that it is absolute, i.e., it completely prevents migration
                of individuals between the two populations on either side of it.

        3.  The establishment of separate populations means that the gene pool of the species as a whole is broken up into two
             independent gene pools.  Each of these gene pools is thus free to evolve as an independent evolutionary unit.

        4.  The populations on either side of the barrier diverge genetically from each other.

            a.  Such divergence may be brought about by genetic drift--different mutations are expected to be fixed by drift in
                 different populations.
            b.  Or, such divergence may be brought about by divergent selection.
                i.  There are likely to be environmental differences on opposite sides of the barrier (e.g., if barrier is mountain range,
                    rainfall differences probably will exist, etc.).
                ii.  As a consequence, these independent gene pools will be subject to different types of selection pressures.
                iii.  Alleles that are favored on one side of the barrier may be disfavored on the other side.
                iv.  Consequently, different patterns of selection will cause different alleles, and hence different traits, to evolve on
                     opposite sides of the barrier.
            c.  Genetic divergence causes the populations to gradually come to differ more and more physiologically,
                 morphologically, and behaviorally.

        5.  If this divergence is allowed to continue long enough, then either or both of two things will occur:

            a.  The genetic makeup of the populations will come to differ sufficiently that hybrid inviability or sterility (post-zygotic
                 isolation) is produced.
            b.  Traits associated with mating behavior will have evolved to be different, so that individuals from the two populations
                 either no longer encounter each other when reproductively active or no longer recognize each other as potential
                 mates.

        6.  Once either of these has occurred, an isolating mechanism is in place, and there can be no exchange of genetic
             material.

        7.  Consequently, when the barrier eventually breaks down, and the two populations are free to intermingle with each
             other, they will be reproductively isolated and hence separate evolutionary lineages.

    C.  Development of hybrid inviability/sterility.

        1.  It is fairly straightforward to envision how divergent natural selection could lead to pre-zygotic reproductive isolation.
             It is perhaps less obvious how post-zygotic isolation evolves.
 

        2.  This is most easily illustrated by a conceptual model.
 

             a.  Consider two enzyme-coding genes, whose enzymes
                  interact in vivo to produce a product.
             b.  For example, many enzymes are known that associate
                  into multi-enzyme complexes (including either homo-
                  or hetero-duplexes) that facilitate the transfer of the
                  reaction product of one enzyme to the next enzyme
                  for which that product serves as a substrate.

        3.  Let the form (nucleotide sequence) of two such genes be
             designated by A and B in the ancestral lineage, and assume
             that these two forms are fixed, so that all individuals are
             AABB.

        4.  Let us postulate that the functionality of the enzyme duplex
             A-B depends on there being a minimal amount of contact
             between specific surfaces x and y of the separate enzymes,
             as depicted in the figure.
 

            a.  Lack of sufficient contact causes the duplex to fall apart, and hence prevents the production of the ultimate
                 biochemical product of the pathway.
            b.  Assuming that this product is "important", lack of sufficient contact will mean a decrease in fitness.

        5.  Now, suppose that in one of the newly independent lineages separated by the physical barrier, natural selection favors
             a modification to the A gene to afford stability at higher temperatures.

            a.  Represent this by the deformation of surface x of the enzyme produced by allele a,(red arrow in  figure).
            b.  Although this change may be beneficial, it may also have the potentially detrimental consequences of reducing the
                 area of contact between enzymes A and B, as shown.
            c.  As long, however, as the area of contact is not reduced below the minimum critical level, duplexes will still form,
                 the benefits of the change will outweigh the costs and natural selection will favor the fixation of allele a in this
                 population.

        6.  Suppose that a similar change occurs in the other population, but in the gene for enzyme B rather than A, and that
             the adaptation is for thermodynamic stability in cold weather.

            a.  Represent this by the deformation of surface y of the enzyme produced by allele b, (blue arrow in figure).
                 Notice that a different section of the area of contact between the enzymes is affected.
            b.  Again, although this change is beneficial, it has the potentially detrimental consequence of reducing the area of
                 contact between enzymes.
            c.  Again, however, as long as the area of contact is not reduced below the minimum critical level, the benefit will
                 outweigh the cost and natural selection will cause the fixation of allele b in the second population.

        7.  In short,

            a.  Population 1 has evolved from AABB  to aaBB.
            b.  Population 2 has evolved from AABB to AAbb.
            c.  In both cases, the enzyme duplex produced is still functional as a duplex.

        8.  Imagine, now, what would happen if the physical barrier broke down, the populations mixed, and mating occurred
             between individuals of the two populations.

            a.  Some of the matings (those between individuals derived from different populations) would be aaBB x AAbb.
            b.  These would produce offspring that were AaBb, in which approximately 1/4 of the enzymes produced would fail to
                 associate (1/4 would associate as A-B duplexes, 1/4 as a-B, 1/4 as A-b, and the remaining quarter, which are a, b,
                 would fail to associate because there is not the needed minimal area of contact between enzymes a and b--see
                 figure).
            c.  In essence, hybrids would produced less of the functional duplex enzyme, which could mean that they would
                 produce less of the important enzyme product, and thus have lower fitness than offspring of within-population
                 matings.

        9.  In many cases, the fitness decriment experienced by hybrids will be small.  However, the summation of a large number
             of small effects of this type associated with divergence in many genes is thought to be sufficient to produce either
             complete hybrid inviability or hybrid sterility.

        10.  Although this model is phrased in terms of natural selection being responsible for divergence in enzyme forms
               between the two populations, such divergence could be achieved by genetic drift as well.

            a.  Thus, imagine that allele a has no effects other than to decrease the area of contact between enzymes.
            b.  If the reduced area of contact between a and B remains sufficient to stabilize the duplex, the fitness of individuals
                 carrying A and individuals carrying a would not be efffected.
            c.  Allele a could then become fixed by drift rather than natural selection.
            d.  In a similar way, b could be fixed by drift in the other population.
            e.  The detrimental consequences to the hybrids would remain, however, since the area of contact between  enzymes a
                 and b would be reduced below the critical threshold needed to maintain duplexes intact.

    D.  Summary

        1.  The allopatric model for the evolution of reproductive isolation postulates that a physical barrier initially causes
             populations to be genetically isolated, thus allowing them to diverge genetically.

        2.  Genetic isolation allows populations to diverge genetically, either due to divergent natural selection or to genetic drift.

        3.  A consequence of genetic divergence is either

            a.  the gradual accumulation of genetic incompatibility, leading to post-zygotic reproductive isolation, or
            b.  gradual divergence in aspects of the mating system (behavior, timing, location of mating), leading to pre-zygotic
                 reproductive isolation.

VII.  Distributional evidence for Allopatric lineage splitting

    A.  Two major types of evidence indicate that Allopatric lineage splitting is common in nature--indeed, probably the most
          prevalent process causing lineage splitting.

        1.  Distributional evidence

        2.  Experimental evidence

    B.  Distributional evidence.

        1.  One type of distributional evidence comes from the observations of naturalists that in many cases, if one examines the
             ranges of what are judged to be closely related species, their ranges do not overlap and are separated by some sort of
             geographic barrier.  This is exactly what would be expected if the species had evolved according to the scenario
             presented earlier.

            a.  Example--Australian tree creepers.
            b.  Example--New Guinea kingishers
 

        2.  A second type of distributional evidence that is used to support the operation of allopatric speciation is the observation
             that isolated island archipellagos are veritable laboratories of speciation.

            a.  Each island of an archipellago or island chain is viewed as being separated by a very effective (though not absolute)
                 barrier to migration (i.e. the ocean).
            b.  Speciation is envisioned to occur as follows:  initially, an ancestral population is present on only one island in the
                 archipellago.
            c.  By some rare chance event, a few individuals are transported from that population to another island, where those
                 individuals become the founders of a new population.
            d.  The two existing populations are isolated by the ocean barrier and allopatric divergence occurs and is accompanied
                 by the evolution of reproductive isolation.
            e.  Each of the daughter lineages may in turn, on rare occasion, contribute to the founding of a new population on
                 another island, which in turn leads to additional lineage splitting and reproductive isolation.
            f.  This process can theoretically continue almost indefinitely to produce a large number of species all descended from
                the same original ancestral species that colonized the island chain.
            g.  This process is also expected to lead to distribution patterns with two distinct features:
                i.  The geographic range of individual lineages will be highly restricted, often to a single island.
                ii.  The ranges of the most closely related species will tend to be disjunct; more specifically, closely related species
                     will tend to occur on different islands, whereas species that share islands will tend to be more distantly related.

        3.  Example--Hawaiian Drosophilids

        4.  Example--Hawaiian Honeycreepers

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