Ecology and population genetics of Sonoran Desert Drosophila

Three species of cactophilic Drosophila endemic to the Sonoran Desert of North America, D. nigrospiracula, D. pachea and D. mettleri, experience marked differences in spatial resource availability, and the first two of these display significant differences in dispersal behaviour. We employed starch gel and cellulose acetate electrophoresis for eight allozyme loci to test for a relationship between these variables and genetic differentiation among geographical populations of each species. No evidence was found for population structure in any of the three species, populations of which were separated by geographical distances of up to 475 km. Allele frequencies for two loci, Mdh-1 and Est-2, in D. nigrospiracula and D. pachea were very similar to those obtained approximately 30 years ago by other workers, indicating that the polymorphisms are remarkably stable under the stressful and variable conditions of the desert environment. High longevity, dispersal and multiple female remating are likely to contribute to the apparent high level of gene flow in all three species.     

Dispersal in cactophilic Drosophila

Three species of Drosophila each breed in necrotic tissue of specific columnar cacti endemic to the Sonoran Desert. Drosophila pachea breeds in senita ( Lophocereus schottii) , D. nigrospiracula breeds in saguaro ( Carnegiea gigantea ) or cardón ( Pachycereus pringlei ), and D. mojavensis uses organ pipe ( Stenocereus thurberi ) in Sonora, Mexico and southern Arizona. Patches of these three host cacti have very different spatial distributions, with those of senita being quite frequent and close together, while those of the other hosts are much father apart. Testing all three species simultaneously, we used capture-mark-release-recapture methods to ask if dispersal differed in these species and if differences were those predicted by the spatial availability of the host patches. D. pachea dispersed the shortest distance in all experiments. Furthermore, D. pachea was the only species showing sex-biased dispersal, with male flies exhibiting the greater propensity to disperse. The observations suggest that across similar spatial scales, D. pachea should show greater population genetic structure than the other two species, and that mitochondrial DNA, because of its maternal inheritance, might show greater evidence of structure than nuclear markers.     

Resource availability and population size in cactophilic Drosophila

1. Four species of Drosophila, Drosophila nigrospiracula ( Patterson & Wheeler 1942 ) , Drosophila mettleri ( Heed 1977 ) , Drosophila pachea ( Patterson & Wheeler 1942 ) , and Drosophila mojavensis ( Patterson & Crow 1940 ) , are endemic to the Sonoran Desert of North America and breed in different species of necrotic columnar cacti. Differences in resource availability have been suggested to explain the interspecific variability in fly population biology, but resource availability for these species has not been quantitatively assessed thoroughly in either spatial or temporal terms. The resource availability was quantified quarterly at three sites for 3 years and population sizes for each Drosophila species were estimated.
2. Spatial and temporal availability of resources differed significantly among species of host cacti, with organpipe cactus ( Stenocereus thurberi ) being the least abundant and senita ( Lophocereus schottii ) the most abundant spatially.
3. Drosophila species differed significantly in population size. The largest population sizes were found for D. nigrospiracula and D. mojavensis and smallest for D. pachea . Populations of D. mettleri were intermediate to these.
4. Population size was greatest for fly species utilizing host species having the largest and longest lasting necroses.
5. Resource availability does not explain the reduction of fly populations in the summer. Necroses were most abundant when flies were absent.     

Resistance to thermal stress in desert Drosophila

1. Four species of Drosophila are endemic to the Sonoran Desert of North America where daily and seasonal high temperatures exceed those experienced by other species in this genus. The close association between these species and their cactus hosts means that they reside only in the desert and raises the question as to whether they are better able to survive heat stress than are non-desert species of Drosophila . The tolerance of adult flies of the four desert species D. mojavensis, D. nigrospiracula, D. pachea and D. mettleri and the cosmopolitan D. simulans to acute heat stress was tested.
2. There was considerable variability among the desert endemic species with respect to survival following heat exposure. Two species, D. mojavensis and D. pachea , were more resistant at 44 °C and 46 °C than the others, with D. mettleri exhibiting similar heat stress resistance to D. simulans .
3. While there was no consistent influence of gender on heat resistance, younger flies (1-day-old) showed significantly greater survival than did older flies (7- or 14-days old).     

Flies across the water: genetic differentiation and reproductive isolation in allopatric desert Drosophila

Between sister species of Drosophila, both pre- and postzygotic reproductive isolation commonly appear by the time a Nei's genetic distance of 0.5 is observed. The degree of genetic differentiation present when allopatric populations of the same Drosophila species exhibit incipient reproductive isolation has not been systematically investigated. Here we compare the relationship between genetic differentiation and pre- and postzygotic isolation among allopatric populations of three cactophilic desert Drosophila: D. mettleri, D. nigrospiracula, and D. mojavensis. The range of all three is interrupted by the Gulf of California, while two species, D. mettleri and D. mojavensis, have additional allopatric populations residing on distant Santa Catalina Island, off the coast of southern California. Significant population structure exists within all three species, but only for allopatric populations of D. mojavensis is significant isolation at the prezygotic level observed. The genetic distances for the relevant populations of D. mojavensis were in the range of 0.12, similar to that for D. mettleri whose greatest D = 0.11 was unassociated with any form of isolation. These observations suggest further investigations of Drosophila populations with genetic distances in this range be undertaken to identify any potential patterns in the relationship between degree of genetic differentiation and the appearance of pre- and/or postzygotic isolation.     

Genetic differentiation and demographic history in Drosophila pachea from the Sonoran Desert

Genetic variation at six microsatellite DNA loci and a segment of the mitochondrial cytochrome oxidase subunit I (COI) locus was used to estimate gene flow, population structure, and demographic history in the cactophilic Drosophila pachea from the Sonoran Desert of North America, a species that shows a strict association with its senita host cactus (genus Lophocereus). For microsatellite analyses, thirteen populations of D. pachea were sampled, five in mainland Mexico and the southwestern USA, and eight on the Baja California (Baja) peninsula, covering essentially the entire range of the species. Analysis of molecular variance (AMOVA) of microsatellite data revealed that populations from both the mainland and the Baja peninsula generally showed little structure, although there were a few exceptions, suggesting some local differentiation and restriction of gene flow within both regions. Pairwise comparisons of F(ST) among each of the mainland and Baja populations showed evidence of both panmixia and population subdivision. AMOVA performed on grouped populations from both the mainland and Baja, however, revealed significant partitioning of genetic variation among the two regions, but no partitioning among localities within each region. Bayesian skyline analyses of the COI data set, consisting of four mainland and seven peninsular populations, revealed population expansions dating to the Pleistocene or late Pliocene in D. pachea from both regions, although regional differences were seen in the estimated timing of the expansions and in changes in effective population size over time.     

Molecular evolution and population genetics of two Drosophila mettleri cytochrome P450 genes involved in host plant utilization

Understanding the genetic basis of adaptation is one of the primary goals of evolutionary biology. The evolution of xenobiotic resistance in insects has proven to be an especially suitable arena for studying the genetics of adaptation, and resistant phenotypes are known to result from both coding and regulatory changes. In this study, we examine the evolutionary history and population genetics of two Drosophila mettleri cytochrome P450 genes that are putatively involved in the detoxification of alkaloids present in two of its cactus hosts: saguaro (Carnegiea gigantea) and senita (Lophocereus schottii). Previous studies demonstrated that Cyp28A1 was highly up-regulated following exposure to rotting senita tissue while Cyp4D10 was highly up-regulated following exposure to rotting saguaro tissue. Here, we show that a subset of sites in Cyp28A1 experienced adaptive evolution specifically in the D. mettleri lineage. Moreover, neutrality tests in several populations were also consistent with a history of selection on Cyp28A1. In contrast, we did not find evidence for positive selection on Cyp4D10, although this certainly does not preclude its involvement in host plant use. A surprising result that emerged from our population genetic analyses was the presence of significant genetic differentiation between flies collected from different host plant species (saguaro and senita) at Organ Pipe National Monument, Arizona, USA. This preliminary evidence suggests that D. mettleri may have evolved into distinctive host races that specialize on different hosts, a possibility that warrants further investigation.     

Phoretic dispersal influences parasite population genetic structure

Dispersal is a fundamental component of the life history of most species. Dispersal influences fitness, population dynamics, gene flow, genetic drift and population genetic structure. Even small differences in dispersal can alter ecological interactions and trigger an evolutionary cascade. Linking such ecological processes with evolutionary patterns is difficult, but can be carried out in the proper comparative context. Here, we investigate how differences in phoretic dispersal influence the population genetic structure of two different parasites of the same host species. We focus on two species of host‐specific feather lice (Phthiraptera: Ischnocera) that co‐occur on feral rock pigeons (Columba livia). Although these lice are ecologically very similar, “wing lice” (Columbicola columbae) disperse phoretically by “hitchhiking” on pigeon flies (Diptera: Hippoboscidae), while “body lice” (Campanulotes compar) do not. Differences in the phoretic dispersal of these species are thought to underlie observed differences in host specificity, as well as the degree of host–parasite cospeciation. These ecological and macroevolutionary patterns suggest that body lice should exhibit more genetic differentiation than wing lice. We tested this prediction among lice on individual birds and among lice on birds from three pigeon flocks. We found higher levels of genetic differentiation in body lice compared to wing lice at two spatial scales. Our results indicate that differences in phoretic dispersal can explain microevolutionary differences in population genetic structure and are consistent with macroevolutionary differences in the degree of host–parasite cospeciation.     

Elemental stoichiometry of Drosophila and their hosts

1. Nitrogen (N) and phosphorus (P) availabilities are important ecological determinants of resource use in nature. Despite the wide range of hosts used by species of the genus Drosophila , elemental composition of natural resources of these flies has never been investigated.
2. Total body N and P contents were determined in seven species of wild-caught Drosophila , their natural hosts, and artificial diets routinely used to rear these flies in the laboratory. The flies tested included D. hydei, D. arizonae, D. simulans and D. pseudoobscura collected from rotting fruit (melons), and the cactophilic D. nigrospiracula, D. mojavensis and D. pachea collected from their specific host plants, Saguaro, Organpipe and Senita cactus, respectively.
3. Natural hosts varied in elemental composition, with fruit showing higher N (2·8–4·3% dry mass) and P (0·50–0·67%) levels compared with cacti (0·5–1·6% N; 0·01–0·29% P). No consistent differences in N and P levels were found between healthy and necrotic cactus tissue.
4. Total body N and P also varied among Drosophila species. This variation mirrored the levels of N and P found in the respective hosts and laboratory diets. N:P ratios were consistently lower in female flies compared with conspecific males suggesting phosphorus demands during oogenesis are high.
5. Potential mechanisms by which Drosophila deal with N or P limitation in nature are discussed.     

The panmixia paradigm of eastern Pacific olive ridley turtles revised: consequences for their conservation and evolutionary biology

Previous studies of the olive ridley Lepidochelys olivacea population structure in the tropical eastern Pacific have indicated the existence of a single panmictic population ranging from Costa Rica to Mexico. This information has been used to design specific management measures to conserve primary nesting beaches in Mexico. However, little is known about olive ridleys in the Baja California Peninsula, their northernmost reproductive limit, where recent observations have shown differences in nesting female behaviour and size of hatchlings relative to other continental rookeries. We used mtDNA control region sequences from 137 turtles from five continental and four peninsular nesting sites to determine whether such differences correspond to a genetic distinction of Baja California olive ridleys or to phenotypic plasticity associated with the extreme environmental nesting conditions of this region. We found that genetic diversity in peninsular turtles was significantly lower than in continental nesting colonies. Analysis of molecular variance revealed a significant population structure (Phi ST = 0.048, P = 0.006) with the inclusion of peninsular samples. Our results: (i) suggest that the observed phenotypic variation may be associated with genetic differentiation and reproductive isolation; (ii) support the recent colonization of the eastern Pacific by Lepidochelys; (iii) reveal genetic signatures of historical expansion and colonization events; and (iv) significantly challenge the notion of a single genetic and conservation unit of olive ridleys in the eastern Pacific. We conclude that conservation measures for olive ridleys in Mexico should be revised to grant peninsular beaches special attention.     

Population structure of African buffalo inferred from mtDNA sequences and microsatellite loci: high variation but low differentiation

The African buffalo ( Syncerus caffer ) is widespread throughout sub-Saharan Africa and is found in most major vegetation types, wherever permanent sources of water are available, making it physically able to disperse through a wide range of habitats. Despite this, the buffalo has been assumed to be strongly philopatric and to form large aggregations that remain within separate home ranges with little interchange between units, but the level of differentiation within the species is unknown. Genetic differences between populations were assessed using mitochondrial DNA (control region) sequence data and analysis of variation at six microsatellite loci among 11 localities in eastern and southern Africa. High levels of genetic variability were found, suggesting that reported severe population bottlenecks due to outbreak of rinderpest during the last century did not strongly reduce the genetic variability within the species. The high level of genetic variation within the species was found to be evenly distributed among populations and only at the continental level were we able to consistently detect significant differentiation, contrasting with the assumed philopatric behaviour of the buffalo. Results of mtDNA and microsatellite data were found to be congruent, disagreeing with the alleged male-biased dispersal. We propose that the observed pattern of the distribution of genetic variation between buffalo populations at the regional level can be caused by fragmentation of a previous panmictic population due to human activity, and at the continental level, reflects an effect of geographical distance between populations.     

Historical vicariance and postglacial colonization effects on the evolution of genetic structure in Lophocereus,a Sonoran Desert columnar cactus

Distinguishing the historical effects of gene migration and vicariance on contemporary genetic structure is problematic without testable biogeographic hypotheses based on preexisting geological and environmental evidence. The availability of such hypotheses for North America's Sonoran Desert has contributed to our understanding of the effect of historical vicariance and dispersal events on the diversification of this region's vertebrate biota but have not yet been applied to its flora. In this paper we describe a detailed allozyme analysis of the population genetic structure and phylogeography of the Sonoran Desert columnar cactus, Lophocereus schottii (senita). Inferred phylogroup distributions reflect two historical vicariance events: (1) a middle Pliocene northward transgression of the Sea of Cortéz that is reflected in well-supported Baja California peninsular and continental phylogroups but not in current taxonomic treatments of the species; and (2) a late Pliocene transpeninsular seaway across southern Baja that is reflected in tentative support for peninsular and southern Cape Region phylogroups corresponding to taxonomic varieties L. schottii var. schottii and L. schottii var. australis, respectively. A middle Pleistocene midpeninsular seaway hypothesized to explain congruent phylogroup distributions in several vertebrate taxa is not reflected in L. s. var. schottii, nor is the distinction of a third variety, L. s. var. tenuis, from continental populations of L. s. var. schottii. Linear regression of pairwise estimates of interpopulation differentiation (M and F(ST)/[1 - F(ST)]) on interpopulation geographic distance revealed significant evidence of isolation by distance within peninsular and continental phylogroups but not between them, consistent with historical vicariance between but not within these regions. We also found significant evidence of isolation by distance between putative L. s. var. schottii and L. s. var. australis phylogroups, suggesting that reproductive isolation between peninsular and Cape Region forms is incomplete. Within peninsular, but not continental, phylogroups, northward range expansion from southern Pleistocene refugia is reflected in significant declines in genetic variation with increasing latitude and in an area phenogram in which populations are progressively nested from south (ancestral) to north (descendant) along the Baja peninsula. Although the geographic concordance of phylogenetic topologies suggests that ancient vicariance events, and not dispersal, have primarily influenced the biogeographic distributions of Baja's vertebrate biota, the phylogeographic structure of L. schottii suggests that Sonoran Desert plant species may exhibit genetic signatures of postglacial range expansion and gene flow as well as vicariance.     

An analysis of genetic differentiation among assortatively mating Drosophila melanogaster in Zimbabwe

African Drosophila melanogaster populations, and those from Zimbabwe in particular, have attracted much interest recently. African flies differ genetically from 'cosmopolitan' populations and were found to exhibit discriminative mating behaviour against individuals from 'cosmopolitan' populations. It has therefore been proposed that Zimbabwean and some other African populations are in an 'incipient stage of speciation'. However, whether the mating behaviour is an effective barrier against gene flow from other populations, and whether intra-population genetic differentiation has already evolved in sympatry is not known. Here, we took a population-based approach to test whether the well-characterized mating type differences have resulted in a genome-wide differentiation at the population level. Using 122 polymorphic microsatellite loci mapping to the third chromosome, we demonstrate a significant genetic differentiation between Zimbabwean flies differing in their mating behaviour. We also provide evidence to suggest that this difference is unlikely to be attributable to population structure within Zimbabwe. However, the analysis of individual microsatellite loci did not indicate more loci differentiating these two groups than expected by chance. Our data suggest that the 'Z'-'M' mating behaviour is strong enough to result in a small but significant genetic differentiation. Thus, future studies based on a larger population sample of flies characterized for their mating behaviour and using more markers are expected to provide more information on the genetic basis of the mating traits in the Zimbabwe flies.     

Linking coevolutionary history to ecological process: doves and lice

Abstract Many host-specific parasites are restricted to a limited range of host species by ecological barriers that impede dispersal and successful establishment. In some cases, microevolutionary differentiation is apparent on top of host specificity, as evidenced by significant parasite population genetic structure among host populations. Ecological barriers responsible for specificity and genetic structure can, in principle, reinforce macroevolutionary processes that generate congruent host-parasite phylogenies. However, few studies have explored both the micro- and macroevolutionary ramifications of close association in a single host-parasite system. Here we compare the macroevolutionary histories of two genera of feather lice (Phthiraptera: Ischnocera) that both parasitize New World pigeons and doves (Aves: Columbiformes). Earlier work has shown that dove body lice (genus Physconelloides ) are more host specific and have greater population genetic structure than dove wing lice ( Columbicola ). We reconstructed phylogenies for representatives of the two genera of lice and their hosts, using nuclear and mitochondrial DNA sequences. The phylogenies were well resolved and generally well supported. We compared the phylogenies of body lice and wing lice to the host phylogeny using reconciliation analyses. We found that dove body lice show strong evidence of cospeciation whereas dove wing lice do not. Although the ecology of body and wing lice is very similar, differences in their dispersal ability may underlie these joint differences in host specificity, population genetic structure, and coevolutionary history.     

Linking behavioral ecology with population genetics: insights from Drosophila nigrospiracula

Although Drosophila species provide important model systems for evolutionary biology, the ecologies and natural histories of most species are insufficiently characterized to permit predictions with respect to issues such as population genetic structure. A notable exception is the group of cactophilic Drosophila endemic to the Sonoran Desert of North America. One of these species, D. nigrospiracula, exhibits no population subdivision anywhere in its range. Here we present evidence suggesting that the timing of mating in relation to dispersal contributes to the panmixia observed in this species.     

Host dispersal as the driver of parasite genetic structure: a paradigm lost?

Understanding traits influencing the distribution of genetic diversity has major ecological and evolutionary implications for host–parasite interactions. The genetic structure of parasites is expected to conform to that of their hosts, because host dispersal is generally assumed to drive parasite dispersal. Here, we used a meta‐analysis to test this paradigm and determine whether traits related to host dispersal correctly predict the spatial co‐distribution of host and parasite genetic variation. We compiled data from empirical work on local adaptation and host–parasite population genetic structure from a wide range of taxonomic groups. We found that genetic differentiation was significantly lower in parasites than in hosts, suggesting that dispersal may often be higher for parasites. A significant correlation in the pairwise genetic differentiation of hosts and parasites was evident, but surprisingly weak. These results were largely explained by parasite reproductive mode, the proportion of free‐living stages in the parasite life cycle and the geographical extent of the study; variables related to host dispersal were poor predictors of genetic patterns. Our results do not dispel the paradigm that parasite population genetic structure depends on host dispersal. Rather, we highlight that alternative factors are also important in driving the co‐distribution of host and parasite genetic variation.     

Genetic differentiation associated with host plants and geography among six widespread species of South American Blepharoneura fruit flies (Tephritidae)

Tropical herbivorous insects are astonishingly diverse, and many are highly host‐specific. Much evidence suggests that herbivorous insect diversity is a function of host plant diversity; yet, the diversity of some lineages exceeds the diversity of plants. Although most species of herbivorous fruit flies in the Neotropical genus Blepharoneura are strongly host‐specific (they deposit their eggs in a single host plant species and flower sex), some species are collected from multiple hosts or flowers and these may represent examples of lineages that are diversifying via changes in host use. Here, we investigate patterns of diversification within six geographically widespread Blepharoneura species that have been collected and reared from at least two host plant species or host plant parts. We use microsatellites to (1) test for evidence of local genetic differentiation associated with different sympatric hosts (different plant species or flower sexes) and (2) examine geographic patterns of genetic differentiation across multiple South American collection sites. In four of the six fly species, we find evidence of local genetic differences between flies collected from different hosts. All six species show evidence of geographic structure, with consistent differences between flies collected in the Guiana Shield and flies collected in Amazonia. Continent‐wide analyses reveal – in all but one instance – that genetically differentiated flies collected in sympatry from different host species or different sex flowers are not one another's closest relatives, indicating that genetic differences often arise in allopatry before, or at least coincident with, the evolution of novel host use.     

Exploring patterns of population subdivision in the net-winged midge, Elporia barnardi (Diptera: Blephariceridae), in mountain streams of the south-western Cape, South Africa

1. The net-winged midges (Diptera: Blephariceridae) are a highly specialized group whose morphological characteristics and specific habitat requirements suggest a limited potential for dispersal. Levels of genetic variation were examined within streams, between streams in the same range and between mountain ranges in larval populations of Elporia barnardi in the south-western Cape of South Africa. The aim was to examine the hypothesis that population structure would reflect the poor potential for dispersal.
2. Significant deviations from Hardy–Weinberg equilibrium in 17 of the 57 individual comparisons indicate a non-random mating population. Given the swarming behaviour and life history traits, larvae sampled may reflect the product of limited matings.
3. Analysis of population substructuring revealed significant levels of differentiation among geographically proximate populations. Large differences between streams within Table Mountain, similar in magnitude to those between mountain ranges, suggest that movement of individuals out of the stream catchment is rare. Observed F _ST values are more similar to those of fully aquatic species than other lotic insects with winged adult stages.
4. Results suggest that mountain ridges provided effective physical barriers to the dispersal of E. barnardi , with the catchment representing the effective population unit.     

Desiccation Resistance in Four Drosophila Species: Sex and Population Effects

Desiccation resistance and body mass were measured in multiple populations of each of four species of Drosophila: two desert endemic species (D. nigrospiracula and D. mojavensis), and two with more widespread distributions (D. melanogaster and D. pseudoobscura). While flies from the desert species were more desiccation tolerant, there was, in certain cases, significant variation in desiccation resistance among populations of the same species. A significant difference in desiccation resistance was observed between the sexes, females were more resistant than males, but this relationship was reversed when taking into account body mass differences between the sexes. The degree of observed within-species variability demonstrates that studies focusing upon differences between species can produce different conclusions if they rely on observations for only single populations of a given species. Our data also suggest the existence of multiple mechanisms for desiccation resistance.     

Beyond the landscape: Resistance modelling infers physical and behavioural gene flow barriers to a mobile carnivore across a metropolitan area

Urbanization affects key aspects of wildlife ecology. Dispersal in urban wildlife species may be impacted by geographical barriers but also by a species’ inherent behavioural variability. There are no functional connectivity analyses using continuous individual‐based sampling across an urban‐rural continuum that would allow a thorough assessment of the relative importance of physical and behavioural dispersal barriers. We used 16 microsatellite loci to genotype 374 red foxes (Vulpes vulpes) from the city of Berlin and surrounding rural regions in Brandenburg in order to study genetic structure and dispersal behaviour of a mobile carnivore across the urban‐rural landscape. We assessed functional connectivity by applying an individual‐based landscape genetic optimization procedure. Three commonly used genetic distance measures yielded different model selection results, with only the results of an eigenvector‐based multivariate analysis reasonably explaining genetic differentiation patterns. Genetic clustering methods and landscape resistance modelling supported the presence of an urban population with reduced dispersal across the city border. Artificial structures (railways, motorways) served as main dispersal corridors within the cityscape, yet urban foxes avoided densely built‐up areas. We show that despite their ubiquitous presence in urban areas, their mobility and behavioural plasticity, foxes were affected in their dispersal by anthropogenic presence. Distinguishing between man‐made structures and sites of human activity, rather than between natural and artificial structures, is thus essential for better understanding urban fox dispersal. This differentiation may also help to understand dispersal of other urban wildlife and to predict how behaviour can shape population genetic structure beyond physical barriers.