John C. Avise

Molecular population structure and the biogeographic history of a regional fauna : a case history with lessons for conservation biology

Mitochondrial (mt) DNA data on the comparative phylogeographic patterns of 19 species of freshwater, coastal, and marine species in the southeastern U.S.A. are reviewed. Nearly all assayed species exhibit extensive mtDNA polymorphism, although still orders-of-magnitude less than predicted under neutrally theory if evolutionary effective population sizes of females are similar to current census sizes. In both the freshwater and marine realms, deep and geographically concordant forks in intraspecific mtDNA phylogenies commonly distinguish regional populations in the Atlantic versus Gulf Coast areas. These concordant phylogeographic patterns among independently evolving species provide evidence of similar vicariant histories of population separation, and can be related tentatively to episodic changes in environmental conditions during the Pleistocene

Microsatellite null alleles in parentage analysis.

Highly polymorphic microsatellite markers are widely employed in population genetic analyses (eg, of biological parentage and mating systems), but one potential drawback is the presence of null alleles that fail to amplify to detected levels in the PCR assays. Here we examine 233 published articles in which authors reported the suspected presence of one or more microsatellite null alleles, and we review how these purported nulls were detected and handled in the data analyses. We also employ computer simulations and analytical treatments to determine how microsatellite null alleles might impact molecular parentage analyses. The results indicate that whereas null alleles in frequencies typically reported in the literature introduce rather inconsequential biases on average exclusion probabilities, they can introduce substantial errors into empirical assessments of specific mating events by leading to high frequencies of false parentage exclusions.

Pleistocene phylogeographic effects on avian populations and the speciation process

Pleistocene biogeographic events have traditionally been ascribed a major role in promoting speciations and in sculpting the present–day diversity and distributions of vertebrate taxa. However, this paradigm has recently come under challenge from a review of interspecific mtDNA genetic distances in birds: most sister–species separations dated to the Pliocene. Here we summarize the literature on intraspecific mtDNA phylogeographic patterns in birds and reinterpret the molecular evidence bearing on Pleistocene influences. At least 37 out of 63 avian species surveyed (59%) are sundered into recognizable phylogeographic units, and 28 of these separations (76%) trace to the Pleistocene. Furthermore, use of phylogroup separation times within species as minimum estimates of ‘speciation durations’ also indicates that many protracted speciations, considered individually, probably extended through time from Pliocene origins to Pleistocene completions. When avian speciation is viewed properly as an extended temporal process rather than as a point event, Pleistocene conditions appear to have played an active role both in initiating major phylogeographic separations within species, and in completing speciations that had been inaugurated earlier. Whether the Pleistocene was exceptional in these regards compared with other geological times remains to be determined.

The use of restriction endonucleases to measure mitochondrial DNA sequence relatedness in natural populations. III. Techniques and potential applications.

SummaryRestriction endonucleases and agarose gel electrophoresis have been used to demonstrate extensive nucleotide sequence diversity in mitochondrial DNA (mtDNA) within and between conspecific populations of rodents and other mammals. Cleavage of mtDNA samples with a relatively small number of endonucleases provides information concerning the phylogenetic relatedness of individual organisms which cannot now be readily obtained by any other type of molecular analysis. This information is qualitatively different from that available from the study of nuclear genes or gene products because the mitochondrial genome is inherited intact from the female parent and is not altered by recombination or meiotic segregation.The requirements for large tissue samples and laborious DNA purification procedures have imposed severe limitations on the kinds of population surveys in which this technique could be utilized. Here, we show that these difficulties can be overcome by using DNA-DNA hybridization to detect minute amounts of mtDNA in crude tissue fractions which can be more easily and rapidly prepared from very small amounts of tissue without the use of expensive and immobile laboratory equipment. The techniques are described in detail in an effort to make restriction analysis of mtDNA available to biologists who may be unfamiliar with current DNA technology.

Speciation durations and Pleistocene effects on vertebrate phylogeography.

An approach applied previously to avian biotas is extended in this paper to other vertebrate classes to evaluate Pleistocene phylogeographic effects and to estimate temporal spans of the speciation process (speciation durations) from mitochondrial (mt) DNA data on extant taxa. Provisional molecular clocks are used to date population separations and to bracket estimates of speciation durations between minimum and maximum values inferred from genetic distances between, respectively, extant pairs of intraspecific phylogroups and sister species. Comparisons of genetic–distance trends across the vertebrate classes reveal the following: (i) speciation durations normally entail at least two million years on average; (ii) for mammals and birds, Pleistocene conditions played an important role in initiating phylogeographic differentiation among now–extant conspecific populations as well as in further sculpting pre–existing phylogeographic variety into many of todays sister species; and (iii) for herpetofauna and fishes, inferred Pleistocene biogeographic influences on present–day taxa differ depending on alternative but currently plausible mtDNA rate calibrations.

Demographic influences on mitochondrial DNA lineage survivorship in animal populations

SummaryProbability models of branching processes and computer simulations of these models are used to examine stochastic survivorship of female lineages under a variety of demographic scenarios. A parameter II, defined as the probability of survival of two or more independent lineages over G generations, is monitored as a function of founding size of a population, population size at carrying capacity, and the frequency distributions of surviving progeny.Stochastic lineage extinction can be very rapid under certain biologically plausible demographic conditions. For stable-sized populations initiated by n females and/or regulated about carrying capacity k=n, it is highly probable that within about 4n generations all descendants will trace their ancestries to a single founder female. For a given mean family size, increased variance decreases lineage survivorship. In expanding populations, however, lineage extinction is dramatically slowed, and the final k value is a far more important determinant of II than is the size of the population at founding. The results are discussed in the context of recent empirical observations of low mitochondrial DNA (mtDNA) sequence heterogeneity in humans and expected distributions of asexually transmitted traits among sexually reproducing species.

GENE TREES AND ORGANISMAL HISTORIES: A PHYLOGENETIC APPROACH TO POPULATION BIOLOGY

A “gene tree” is the phylogeny of alleles or haplotypes for any specified stretch of DNA. Gene trees are components of population trees or species trees; their analysis entails a shift in perspective from many of the familiar models and concepts of population genetics, which typically deal with frequencies of phylogenetically unordered alleles. Molecular surveys of haplotype diversity in mitochondrial DNA (mtDNA) have provided the first extensive empirical data suitable for estimation of gene trees on a microevolutionary (intraspecific) scale. The relationship between phylogeny and geographic distribution constitutes the phylogeographic pattern for any species. Observed phylogeographic trees can be interpreted in terms of historical demography by comparison to predictions derived from models of gene lineage sorting, such as inbreeding theory and branching‐process theory. Results of such analyses for more than 20 vertebrate species strongly suggest that the demographies of populations have been remarkably dynamic and unsettled over space and recent evolutionary time. This conclusion is consistent with ecological observations documenting dramatic population‐size fluctuations and range shifts in many contemporary species. By adding an historical perspective to population biology, the gene‐lineage approach can help forge links between the disciplines of phylogenetic systematics (and macroevolutionary study) and population genetics (microevolution). Preliminary extensions of the “gene tree” methodology to haplotypes of nuclear genes (such as Adh in Drosophila melanogaster) demonstrate that the phylogenetic perspective can also help to illuminate molecular‐genetic processes (such as recombination or gene conversion), as well as contribute to knowledge of the origin, age, and molecular basis of particular adaptations.

The history and purview of phylogeography: a personal reflection

Last year marked the 10th anniversary of the birth of phylogeography as a formal discipline. However, the field’s gestation began in the mid‐1970s with the introduction of mitochondrial (mt) DNA analyses to population genetics, and to the profound shift toward genealogical thought at the intraspecific level (now formalized as coalescent theory) that these methods prompted. This paper traces the early history and explosive growth of phylogeography, and closes with predictions about future challenges for the field that centre on several facets of genealogical concordance.

Global population structure and natural history of the green turtle chelonia mydas in terms of matriarchal phylogeny

To address aspects of the evolution and natural history of green turtles, we assayed mitochondrial (mt) DNA genotypes from 226 specimens representing 15 major rookeries around the world. Phylogenetic analyses of these data revealed (1) a comparatively low level of mtDNA variability and a slow mtDNA evolutionary rate (relative to estimates for many other vertebrates); (2) a fundamental phylogenetic split distinguishing all green turtles in the Atlantic‐Mediterranean from those in the Indian‐Pacific Oceans; (3) no evidence for matrilineal distinctiveness of a commonly recognized taxonomic form in the East Pacific (the black turtle C.m. agassizi or C. agassizi); (4) in opposition to published hypotheses, a recent origin for the Ascension Island rookery, and its close genetic relationship to a geographically proximate rookery in Brazil; and (5) a geographic population substructure within each ocean basin (typically involving fixed or nearly fixed genotypic differences between nesting populations) that suggests a strong propensity for natal homing by females. Overall, the global matriarchal phylogeny of Chelonia mydas appears to have been shaped by both geography (ocean basin separations) and behavior (natal homing on regional or rookery‐specific scales). The shallow evolutionary population structure within ocean basins likely results from demographic turnover (extinction and colonization) of rookeries over time frames that are short by evolutionary standards but long by ecological standards.

EVOLUTIONARY GENETICS OF CAVE-DWELLING FISHES OF THE GENUS ASTYANAX

Attempts to understand evolutionary processes in cave organisms have been largely limited to speculation on the causes of loss of photoreceptor organs and pigmentation, increase in size and complexity of tactile sensory structures, and certain modifications in physiology (see review in Barr, 1968). Little is known of the population genetics of cave organisms or of the genetic changes accompanying the transformation of epigean (surface-dwelling) forms to troglobites (obligate cavernicoles). Yet genetic information is essential to the confident development of theories of troglobite evolution. For this reason, we have compared the genic character and degree of variability in troglobitic and epigean populations of the characid fish Astyanax mexicanus in Mexico. Students of cave biology have generally accepted the thesis that the ancestors of many troglobites entered caves as troglophiles (facultative cavernicoles) before the end of the Pleistocene, and became isolated with the local extinction of surface populations as a result of climatic changes associated with glaciation (Barr, 1968). If this is true, many troglobites have been living