Benjamin M. Fitzpatrick

Recent divergence with gene flow in Tennessee cave salamanders (Plethodontidae: Gyrinophilus) inferred from gene genealogies.

Cave organisms occupy a special place in evolutionary biology because convergent morphologies of many species demonstrate repeatability in evolution even as they obscure phylogenetic relationships. The origin of specialized cave‐dwelling species also raises the issue of the relative importance of isolation vs. natural selection in speciation. Two alternative hypotheses describe the origin of subterranean species. The ‘climate‐relict’ model proposes allopatric speciation after populations of cold‐adapted species become stranded in caves due to climate change. The ‘adaptive‐shift’ model proposes parapatric speciation driven by divergent selection between subterranean and surface habitats. Our study of the Tennessee cave salamander complex shows that the three nominal forms (Gyrinophilus palleucus palleucus, G. p. necturoides, and G. gulolineatus) arose recently and are genealogically nested within the epigean (surface‐dwelling) species, G. porphyriticus. Short branch lengths and discordant gene trees were consistent with a complex history involving gene flow between diverging forms. Results of coalescent‐based analysis of the distribution of haplotypes among groups reject the allopatric speciation model and support continuous or recurrent genetic exchange during divergence. These results strongly favour the hypothesis that Tennessee cave salamanders originated from spring salamanders via divergence with gene flow.

Rapid spread of invasive genes into a threatened native species.

When introduced or cultivated plants or animals hybridize with their native relatives, the spread of invasive genes into native populations might have biological, aesthetic, and legal implications. Models suggest that the rate of displacement of native by invasive alleles can be rapid and inevitable if they are favored by natural selection. We document the spread of a few introduced genes 90 km into a threatened native species (the California Tiger Salamander) in 60 years. Meanwhile, a majority of genetic markers (65 of 68) show little evidence of spread beyond the region where introductions occurred. Using computer simulations, we found that such a pattern is unlikely to emerge by chance among selectively neutral markers. Therefore, our results imply that natural selection has favored both the movement and fixation of these exceptional invasive alleles. The legal status of introgressed populations (native populations that are slightly genetically modified) is unresolved by the US Endangered Species Act. Our results illustrate that genetic and ecological factors need to be carefully weighed when considering different criteria for protection, because different rules could result in dramatically different geographic areas and numbers of individuals being protected.

What, if anything, is sympatric speciation?

Sympatric speciation has always fascinated evolutionary biologists, and for good reason; it pits diversifying selection directly against the tendency of sexual reproduction to homogenize populations. However, different investigators have used different definitions of sympatric speciation and different criteria for diagnosing cases of sympatric speciation. Here, we explore some of the definitions that have been used in empirical and theoretical studies. Definitions based on biogeography do not always produce the same conclusions as definitions based on population genetics. The most precise definitions make sympatric speciation an infinitesimal end point of a continuum. Because it is virtually impossible to demonstrate the occurrence of such a theoretical extreme, we argue that testing whether a case fits a particular definition is less informative than evaluating the biological processes affecting divergence. We do not deny the importance of geographical context for understanding divergence. Rather, we believe this context can be better understood by modelling and measuring quantities, such as gene flow and selection, rather than assigning cases to discrete categories like sympatric and allopatric speciation.

THE GEOGRAPHY OF MAMMALIAN SPECIATION: MIXED SIGNALS FROM PHYLOGENIES AND RANGE MAPS

Abstract The importance of geographic isolation in speciation has been debated since the 19th century. Since the beginning of the 20th century, the consensus has been that most speciation involves divergence in allopatry. This consensus was based largely on decades of observations by naturalists and verbal arguments against speciation without isolation. Recent attempts to quantify the importance of allopatric versus sympatric speciation using comparative methods called “age‐range correlation” (ARC) suggest that allopatric speciation is more common than sympatric speciation. However, very few taxa have been studied and there are concerns about the adequacy of the methods. We propose methodological improvements including changes in the way overlap between clades is quantified and Monte Carlo methods to test the null hypothesis of no relationship between phylogenetic relatedness and geographic range overlap. We analyze 14 clades of mammals, chosen because of the availability of data and the consensus among mammalogists that speciation is routinely allopatric. Although data from a few clades clearly indicate allopatric speciation, divergence with gene flow is plausible in others and many results are inconclusive. The relative rarity of significant correlations between phylogenetic distance and range overlap may have three distinct causes: (1) postspeciation range changes, (2) relative rarity of range overlap, and (3) a mixture of geographic modes of speciation. Our results support skepticism about ARCs power for inferring the biogeography of speciation. Yet, even if few clades provide clear signals, meta‐analytic approaches such as ARC may set bounds on the prevalence of alternative modes of speciation.

Assortative mating in poison-dart frogs based on an ecologically important trait

Abstract The origin of new species can be influenced by both deterministic and stochastic factors. Mate choice and natural selection may be important deterministic causes of speciation (as opposed to the essentially stochastic factors of geographic isolation and genetic drift). Theoretical models predict that speciation is more likely when mate choice depends on an ecologically important trait that is subject to divergent natural selection, although many authors have considered such mating/ecology pleiotropy, or “magic-traits” to be unlikely. However, phenotypic signals are important in both mate choice and ecological processes such as avoiding predation. In chemically defended species, it may be that the phenotypic characteristics influencing mate choice are the same signals being used to transmit a warning to potential predators, although few studies have demonstrated this in wild populations. We tested for assortative mating between two color morphs of the Strawberry Poison-Dart Frog, Dendrobates pumilio, a group with striking geographic variation in aposematic color patterns. We found that females significantly prefer individuals of their own morph under two different light treatments, indicating strong assortative mating based on multiple coloration cues that are also important ecological signals. This study provides a rare example of one phenotypic trait affecting both ecological viability and nonrandom mating, indicating that mating/ecology pleiotropy is plausible in wild populations, particularly for organisms that are aposematically colored and visually orienting.

Rates of evolution of hybrid inviability in birds and mammals.

Abstract Almost 30 years ago, A. C. Wilson and colleagues presented results indicating that hybrid inviability between species evolves 10 times faster in mammals than in birds and frogs. Here I revisit this question for birds and mammals using modern molecular data (mitochondrial cytochrome b DNA) and a more phylogenetically appropriate statistical approach. My analyses confirm that diverging mammals lose the ability to form viable hybrids faster than birds. To explain the difference in rates of evolutionary loss of hybridization potential, Wilson and coworkers proposed that mammals have higher rates of regulatory evolution, causing higher probabilities of developmental incompatibilities between mammal species. I briefly discuss this and other potential explanations.

What can DNA tell us about biological invasions

It is often hoped that population genetics can answer questions about the demographic and geographic dynamics of recent biological invasions. Conversely, invasions with well-known histories are sometimes billed as opportunities to test methods of population genetic inference. In both cases, underappreciated limitations constrain the usefulness of genetic methods. The most significant is that human-caused invasions have occurred on historical timescales that are orders of magnitude smaller than the timescales of mutation and genetic drift for most multicellular organisms. Analyses based on the neutral theory of molecular evolution cannot resolve such rapid dynamics. Invasion histories cannot be reconstructed in the same way as biogeographic changes occurring over millenia. Analyses assuming equilibrium between mutation, drift, gene flow, and selection will rarely be applicable, and even methods designed for explicitly non-equilibrium questions often require longer timescales than the few generations of most invasions of current concern. We identified only a few population genetic questions that are tractable over such short timescales. These include comparison of alternative hypotheses for the geographic origin of an invasion, testing for bottlenecks, and hybridization between native and invasive species. When proposing population genetic analysis of a biological invasion, we recommend that biologists ask (i) whether the questions to be addressed will materially affect management practice or policy, and (ii) whether the proposed analyses can really be expected to address important population genetic questions. Despite our own enthusiasm for population genetic research, we conclude that genetic analysis of biological invasions is justified only under exceptional circumstances.

Pattern, process and geographic modes of speciation

The tradition of classifying cases of speciation into discrete geographic categories (allopatric, parapatric and sympatric) fuelled decades of fruitful research and debate. Not surprisingly, as the science has become more sophisticated, this simplistic taxonomy has become increasingly obsolete. Geographic patterns are now reasonably well understood. Sister species are rarely sympatric, implying that sympatric speciation, it its most general sense, is rare. However, sympatric speciation, even in its most restricted population genetic sense, is possible. Several case studies have demonstrated that divergence has occurred in nature without geographic barriers to gene flow. Obviously, different sets of criteria for sympatric speciation will lead to different numbers of qualifying cases. But changing the rules of nomenclature to make ‘sympatric speciation’ more or less common does not constitute scientific progress. Advances in the study of speciation have come from studies of the processes that constrain or promote divergence, and how they are affected by geography.

Delimiting species using multilocus data: Diagnosing cryptic diversity in the southern cavefish, typhlichthys subterraneus (teleostei: Amblyopsidae)

A major challenge facing biodiversity conservation and management is that a significant portion of species diversity remains undiscovered or undescribed. This is particularly evident in subterranean animals in which species delimitation based on morphology is difficult because differentiation is often obscured by phenotypic convergence. Multilocus genetic data constitute a valuable source of information for species delimitation in such organisms, but until recently, few methods were available to objectively test species delimitation hypotheses using genetic data. Here, we use recently developed methods for discovering and testing species boundaries and relationships using a multilocus dataset in a widely distributed subterranean teleost fish, Typhlichthys subterraneus, endemic to Eastern North America. We provide evidence that species diversity in T. subterraneus is currently underestimated and that the picture of a single, widely distributed species is not supported. Rather, several morphologically cryptic lineages comprise the diversity in this clade, including support for the recognition of T. eigenmanni. The high number of cryptic species in Typhlichthys highlights the utility of multilocus genetic data in delimiting species, particularly in lineages that exhibit slight morphological disparity, such as subterranean organisms. However, results depend on sampling of individuals and loci; this issue needs further study.

HYBRIDIZATION BETWEEN A RARE, NATIVE TIGER SALAMANDER (AMBYSTOMA CALIFORNIENSE) AND ITS INTRODUCED CONGENER

Exotic species threaten native biodiversity through predation, competition, and habitat alteration, but also by hybridizing with native species. A lack of reproductive isolation between exotic and native species can lead to genetic swamping, loss of native genetic diversity, and, in rare or endangered species, extirpation or extinction. We examined hybridization between a declining native salamander, the California tiger salamander, Am- bystoma californiense, and an introduced congener, A. tigrinum. Ambystoma californiense is restricted to central California where A. tigrinum has been deliberately introduced as fish bait. In the Salinas Valley, we sampled salamanders from four artificial ponds and two natural vernal pools. Based on mitochondrial DNA and two nuclear loci, we found that hybrids were present in all six ponds, and that these hybrids were viable and fertile. No potentially pure A. californiense were present in three of the six ponds, and only one pond had more than 8% possibly pure native animals. Despite a relatively ancient split and wide genetic divergence between these taxa, they are interbreeding and threatening the genetic purity of the native species. Our data also suggest that the extent of the genetic mixing depends on the breeding habitat. There is little evidence of barriers to gene exchange in the four artificial breeding ponds. However in the two vernal pools, we found significantly fewer larvae with hybrid genotypes and significantly more with pure parental genotypes than expected. Linkage disequilibria revealed positive associations between native alleles and genotypes, and neg- ative associations between native and introduced alleles and genotypes in these two ponds. Despite rampant hybridization, these data provide evidence of some constraints on hy- bridization in the native breeding habitats. Our results suggest that habitat characteristics of native species should be exploited in management strategies to limit hybridization with exotics.