Carla Hurt

Frequency-dependent survival in natural guppy populations

The maintenance of genetic variation in traits under natural selection is a long-standing paradox in evolutionary biology. Of the processes capable of maintaining variation, negative frequency-dependent selection (where rare types are favoured by selection) is the most powerful, at least in theory; however, few experimental studies have confirmed that this process operates in nature. One of the most extreme, unexplained genetic polymorphisms is seen in the colour patterns of male guppies (Poecilia reticulata). Here we manipulated the frequencies of males with different colour patterns in three natural populations to estimate survival rates, and found that rare phenotypes had a highly significant survival advantage compared to common phenotypes. Evidence from humans and other species implicates frequency-dependent survival in the maintenance of molecular, morphological and health-related polymorphisms. As a controlled manipulation in nature, this study provides unequivocal support for frequency-dependent survival—an evolutionary process capable of maintaining extreme polymorphism.

Genetic divergence, population structure and historical demography of rare springsnails (Pyrgulopsis) in the lower Colorado River basin

Springsnails of the genus Pyrgulopsis are the most diverse group of freshwater gastropods in North America and current estimates show that Pyrgulopsis contains ~120 different species, many of which are at risk of extinction. Some factors contributing to their exceptional diversity include poor dispersal ability and extreme habitat specificity based on water availability, chemistry and depth. Most taxa exhibit high degrees of endemism, with many species occurring only in a single spring or seep, making springsnails ideal for studies of speciation and population structure. Here I present data from a survey of genetic variation at the mitochondrial gene cytochrome oxidase I from 37 populations and over 1000 individuals belonging to 16 species of Pyrgulopsis distributed throughout the lower Colorado River basin. High levels of interspecific sequence divergence indicate that Pyrgulopsis may have colonized this region multiple times beginning in the late Miocene (~6 Ma); earlier than previous estimates based on fossil evidence. Estimates of nucleotide diversity differ greatly among species and may reflect differences in demographic processes. These results are used to identify factors contributing to radiation of species in this region. The implications of this evolutionary history and genetic variation are discussed in relation to future management and conservation.

A MULTILOCUS TEST OF SIMULTANEOUS DIVERGENCE ACROSS THE ISTHMUS OF PANAMA USING SNAPPING SHRIMP IN THE GENUS ALPHEUS

The completion of the Panamanian Isthmus is one of the greatest natural experiments in evolution, sending multiple species pairs from a broad range of taxonomic groups on independent evolutionary trajectories. The resulting transisthmian sister species have been used as model systems for examining consequences that accompany cessation of gene flow in formerly panmictic populations. However, variance in pairwise genetic distances of these “geminates” often exceeds expectations, seemingly conflicting with the assumption that separation of populations was contemporaneous with the final closure of the Isthmus. Multilocus datasets and coalescent-based analytical methods can be used to estimate divergence times while accounting for variance in gene divergence that predates isolation, thus removing the need to invoke unequal divergence times. Here we present results from Bayesian analyses of sequence data from seven nuclear and one mitochondrial marker in eight transisthmian species pairs in the snapping shrimp genus Alpheus. Divergence times in two species pairs were shown to occur much earlier than the Isthmus final closure, but much of the variance in pairwise genetic distances from cytochrome oxidase I (COI) was explained when ancestral polymorphisms were accounted for. Results illustrate how coalescent approaches may be more appropriate for dating recent divergences than for estimating ancient speciation events.

Conservation genetics in aquatic species: General approaches and case studies in fishes and springsnails of arid lands

Abstract.Many aquatic species have become endangered because of the elimination and fragmentation of their habitat, human alteration of the environment, and introduced species. New applications and insights from genetic studies of endangered species are being used to formulate management plans to prevent extinction of endangered taxa. Here we discuss three applications of genetic techniques to the conservation of endangered aquatic species in the desert Southwest, USA. First, we discuss estimation of long-term effective population size in three endangered big-river fishes, bonytail chub (Gila elegans), humpback chub (G. cypha) and razorback suckers (Xyrauchen texanus), of the lower Colorado River. For all three species, the current census number is much smaller than the estimated effective population size in which these species evolved. Second, we discuss the determination of species, ESUs, and MUs in the endangered Sonoran topminnow. Molecular genetic data show that the Gila and Yaqui topminnows are different species. Experimental examination of pre-mating and post-mating reproductive isolation demonstrates that some reproductive isolation has already developed between these two species. Finally, springsnails (Pyrgulopsis) of the lower Colorado River basin exist only in remote and isolated springs. Examination of molecular variation generally supports the morphological designation of 16 different species, although a few species have several ESUs. There does not appear to be a correlation of genetic and geographic distance between species, suggesting that they are quite old. These genetic studies provide insight into the conservation of these rare aquatic species. Although mitigating ecological factors may be most significant in preventing extinction, genetic studies can provide the evolutionary context for endangered species and identify what units are most in need of conservation.

Phylogenetic relationships within the snapping shrimp genus Synalpheus (Decapoda: Alpheidae)

The snapping shrimp genus Synalpheus (Alpheidae) is one of the most speciose decapod genera, with over 160 described species worldwide. Most species live in symbiotic relationships with other marine organisms, such as sponges, corals and crinoids, and some sponge-dwelling species have a highly organized, social structure. The present study is the first worldwide molecular phylogenetic analysis of Synalpheus, based on >2,200 bp of sequence data from two mitochondrial (COI and 16S) and two nuclear (PEPCK and 18S) loci. Our molecular data show strong support for monophyly of three out of six traditionally recognized morphology-based species groups: the S. brevicarpus, S. comatularum and S. gambarelloides groups. The remaining three species groups (S. paulsoni, S. neomeris and S. coutierei groups) are non-monophyletic in their current composition and will need to be either abandoned or taxonomically redefined. We also identified potential cryptic species of Synalpheus in our dataset, using intraspecific and interspecific sequence variation in COI from the taxonomically well-studied S. gambarelloides group to establish a genetic divergence threshold. We then used both genetic divergence and tree-based criteria (reciprocal monophyly) to identify potential cryptic species in the remaining taxa of the genus. Our results suggest the presence of multiple cryptic lineages in Synalpheus, underlining the need for more integrative taxonomic studies-including morphological, ecological, molecular, and color pattern data-in this biologically interesting genus.

Revision of the Alpheus cristulifrons species complex (Crustacea: Decapoda: Alpheidae), with description of a new species from the tropical eastern Atlantic

The taxonomy of the snapping shrimp Alpheus cristulifrons Rathbun, 1900, previously reported from the eastern Pacific and western and eastern Atlantic, is reviewed based on molecular data (COI), morphology and colour patterns. Three species are recognized in the A. cristulifrons species complex. Alpheus cristulifrons sensu stricto is restricted to the western Atlantic, ranging from Florida and the Caribbean Sea to southern Brazil. The eastern Pacific A. cristulifrons sensu Kim & Abele, 1988 corresponds to A. utriensis Ramos & Von Prahl, 1989, ranging from the Gulf of California to Colombia; this species can be separated from A. cristulifrons by the absence of balaeniceps setae on the male minor chela and the presence of bands on the antennular and antennal flagella. The eastern Atlantic A. cristulifrons sensu Crosnier & Forest, 1966 is described as A. xanthocarpus sp. nov. based on recently collected material from the island of Sao Tome in the Gulf of Guinea; this species differs from A. cristulifrons by the posteriorly more extending rostral carina and the presence of conspicuous yellow spots on the carpus and chela of the second pereiopod. Molecular data suggest that A. utriensis is the eastern Pacific sister clade to the amphi-Atlntic clade that includes A. cristulifrons and A. xanthocarpus sp. nov.

Ecological speciation in anemone-associated snapping shrimps (Alpheus armatus species complex).

Divergent natural selection driven by competition for limited resources can promote speciation, even in the presence of gene flow. Reproductive isolation is more likely to result from divergent selection when the partitioned resource is closely linked to mating. Obligate symbiosis and host fidelity (mating on or near the host) can provide this link, creating ideal conditions for speciation in the absence of physical barriers to dispersal. Symbiotic organisms often experience competition for hosts, and host fidelity ensures that divergent selection for a specific host or host habitat can lead to speciation and strengthen pre‐existing reproductive barriers. Here, we present evidence that diversification of a sympatric species complex occurred despite the potential for gene flow and that partitioning of host resources (both by species and by host habitat) has contributed to this diversification. Four species of snapping shrimps (Alpheus armatus, A. immaculatus, A. polystictus and A. roquensis) are distributed mainly sympatrically in the Caribbean, while the fifth species (A. rudolphi) is restricted to Brazil. All five species are obligate commensals of sea anemones with a high degree of fidelity and ecological specificity for host species and habitat. We analysed sequence data from 10 nuclear genes and the mitochondrial COI gene in 11–16 individuals from each of the Caribbean taxa and from the only available specimen of the Brazilian taxon. Phylogenetic analyses support morphology‐based species assignments and a well‐supported Caribbean clade. The Brazilian A. rudolphi is recovered as an outgroup to the Caribbean taxa. Isolation–migration coalescent analysis provides evidence for historical gene flow among sympatric sister species. Our data suggest that both selection for a novel host and selection for host microhabitat may have promoted diversification of this complex despite gene flow.

The endangered Sonoran topminnow: Examination of species and ESUs using three mtDNA genes

There has been controversy over the species status of Sonoran topminnows and debate about the presence of ESUs in the Gila topminnow. From examination of sequence variation at 2626 base pairs over three mtDNA genes, we found a 29 (1.1%) nucleotide genetic difference between Gila and Yaqui topminnows. This provides strong support that these two taxa are separate species, Poeciliopsis occidentalis (Gila topminnow) and P. sonoriensis (Yaqui topminnow) and have been separated for approximately one million years. All the Gila topminnows within Arizona have the same sequence for the three mtDNA genes, that is, there is not reciprocal monophyly for mtDNA sequence data for the two previously designated ESUs. However, evidence of the unique habitat for Monkey Spring, its long-term isolation from other Gila topminnow habitats, and the presence of unique fish and invertebrate taxa in Monkey Spring support the designation of the Monkey Spring topminnows as an ESU. Finally, theoretical considerations using molecular data and estimates of heterozygosity and genetic distance for nuclear genes between populations of the Gila topminnow show that the lack of mtDNA variation is not inconsistent with the level and pattern of nuclear genetic variation observed.

Mating behaviour in the endangered Sonoran topminnow: speciation in action

Two species of the endangered Sonoran topminnow, Poeciliopsis occidentalis and P. sonoriensis, occur in two isolated drainage systems in southeast Arizona, U.S.A., and are allopatric throughout their range. Although these two taxa are morphologically very similar, and have been previously described as the same species or subspecies, several molecular studies have since indicated that they differ more than their morphology suggests. To determine whether the behaviours of the two species function as premating barriers to reproduction, we investigated their mating preferences and behavioural patterns in a laboratory setting. Results from no-choice mating observations showed that the mating behaviours of the two species differ. Observations conducted during multiple-choice mating trials provided evidence of assortative mating, suggesting an early stage of premating reproductive isolation.

INITIAL STAGES OF REPRODUCTIVE ISOLATION IN TWO SPECIES OF THE ENDANGERED SONORAN TOPMINNOW

Abstract Long‐term geographic isolation can result in reproductive incompatibilities due to forces such as mutation, genetic drift, and differential selection. In the Sonoran topminnow, molecular genetic studies of mtDNA, microsatellites, and MHC genes have shown that the endangered Gila and Yaqui topminnows are substantially different, suggesting that divergence took place approximately two million years ago. Here we examined hybrid crosses and backcrosses between these two allopatric taxa to evaluate the accumulation of postmating barriers to reproduction. These results are then compared with results from a previous study where male topminnows were shown to mate assortatively with conspecific females. Despite their preference for conspecific mates, both types of interspecific crosses successfully produced offspring. There was evidence of reduced hybrid fitness, including smaller mean brood size and male‐biased sex ratio, for some classes of backcrosses. Brood sizes and interbrood intervals varied significantly when hybrids were subdivided into different cross categories. Our results illustrate the importance of distinctly defining hybrid classes in studies of reproductive isolation. To our knowledge, this is the first such detailed evolutionary analysis in endangered fish taxa.