Notes and Comments Invertebrate Eggs Can Fly: Evidence of Waterfowl-Mediated Gene Flow in Aquatic Invertebrates (original) (raw)
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Invertebrate Eggs Can Fly: Evidence of Waterfowl‐Mediated Gene Flow in Aquatic Invertebrates
The American Naturalist, 2005
Waterfowl often have been assumed to disperse freshwater aquatic organisms between isolated wetlands, but no one has analyzed the impact of this transport on the population structure of aquatic organisms. For three cladocerans (Daphnia ambigua, Daphnia laevis, and Sida crystallina) and one bryozoan (Cristatella mucedo), we estimated the genetic distances between populations across North America using sequences of several mitochondrial DNA genes and genotypic frequencies at allozyme and microsatellite loci. Waterfowl movements across North America (estimated from band recovery data) explained a significant proportion of the gene flow occurring between populations across the continent for three of the four species, even after controlling for geographic distances between localities. The fourth species, S. crystallina, has propagules less likely to survive desiccation or ingestion by birds. Differences in the capacity to exploit bird-mediated transport are likely to have important consequences for the ecology of aquatic communities and the spread of invasive species.
Journal of the North American Benthological Society, 2010
Whether active or passive, dispersal accompanied by gene flow shapes the genetic makeup of populations and ultimately the evolutionary divergence of species. Our objective was to determine if 2 very different aquatic invertebrates with overlapping distributions show similar dispersal histories in their phylogeographic patterns and genetic uniqueness. Two spring-dwelling invertebrates, Hyalella azteca and Callibaetis americanus, were collected from 6 adjacent closed basins in the Great Basin of western North America. Cytochrome c oxidase subunit I (COI) and the 28S ribosomal subunit were used as genetic markers in Hyalella, and COI with the 16S ribosomal subunit of the mitochondrial genome were examined in Callibaetis. Maximum parsimony (MP) and likelihood (ML) analyses, F ST values, analysis of molecular variance (AMOVA), Mantel tests, and nested clade phylogeographical analysis (NCPA) were used to evaluate geographical associations. Hyalella azteca appears to have been in the adjacent basins much longer than has Callibaetis. F ST values in H. azteca reached near fixation. Callibaetis americanus F ST values were lower suggesting greater gene flow and, consequently, higher dispersal rates. Mantel tests did not detect significant isolation by distance for either species, but NCPA on smaller networks of closely related haplotypes found the genetic structure in C. americanus dominated by restricted gene flow with isolation by distance. Hyalella azteca was characterized more by gradual range expansion followed by fragmentation. These results suggest that these isolated freshwater communities are amalgams of species that entered at different times, with weak dispersers having greater constraints on movement and, thus, reflecting an older geographical story than do species with stronger dispersal capabilities.
PeerJ 1: e200. DOI 10.7717/peerj.200, 2013
Since Darwin’s time, waterbirds have been considered an important vector for the dispersal of continental aquatic invertebrates. Bird movements have facilitated the worldwide invasion of the American brine shrimp Artemia franciscana, transporting cysts (diapausing eggs), and favouring rapid range expansions from introduction sites. Here we address the impact of bird migratory flyways on the population genetic structure and phylogeography of A. franciscana in its native range in the Americas. We examined the sequence variation for two mitochondrial gene fragments (COI and 16S for a subset of the data) in a large set of population samples representing the entire native range of A. franciscana. Furthermore, we performed Mantel tests and redundancy analyses (RDA) to test the role of flyways, geography and human introductions on the phylogeography and population genetic structure at a continental scale. A. franciscana mitochondrial DNA was very diverse, with two main clades, largely corresponding to Pacific and Atlantic populations, mirroring American bird flyways. There was a high degree of regional endemism, with populations subdivided into at least 12 divergent, geographically restricted and largely allopatric mitochondrial lineages, and high levels of population structure ( Φ ST of 0.92), indicating low ongoing gene flow. We found evidence of human-mediated introductions in nine out of 39 populations analysed. Once these populations were removed, Mantel tests revealed a strong association between genetic variation and geographic distance (i.e., isolation-by-distance pattern). RDA showed that shared bird flyways explained around 20% of the variance in genetic distance between populations and this was highly significant, once geographic distance was controlled for. The variance explained increased to 30% when the factor human introduction was included in the model. Our findings suggest that bird-mediated transport of brine shrimp propagules does not result in substantial ongoing gene flow; instead, it had a significant historical role on the current species phylogeography, facilitating the colonisation of new aquatic environments as they become available along their main migratory flyways.
2016
Little is known about the life histories, population connectivity, or dispersal mechanisms of shallow groundwater organisms. Here we used RAD-seq to analyze population structure in two aquifer species: Paraperla frontalis, a stonefly with groundwater larvae and aerial adults, and Stygobromus sp., a groundwater-obligate amphipod. We found similar levels of connectivity in each species between floodplains separated by ~70 river km in the Flathead River basin of NW Montana, USA. Given that Stygobromous lacks the aboveground life stage of P. frontalis, our findings suggest that aquifer-obligate species might have previously unrecognized dispersal capacity. 1. Introduction In 1974, Stanford and Gaufin [1] reported stoneflies in an alluvial aquifer supplying domestic water to a Montana community. Researchers have since documented diverse communities of macroinvertebrates, meiofauna, and microbes in shallow aquifers worldwide, and explored the conservation and ecological importance of floodplain habitats [e.g., 2,3]. These communities include insects that spend time above ground (amphibionts), as well as taxa (e.g. crustaceans, oligochaetes, and mites) that never leave interstitial spaces in aquifers (stygobionts). These animals occur up to 10 meters beneath riverine floodplains and as many as two km from the main river channels [4]. Amphibiotic stoneflies spend 1-3 years maturing in the aquifer before emerging as adults with an aerial lifespan of only a few days [5]. The life cycles of many stygobionts, including Stygobromus, are largely unknown. Shallow aquifers offer many challenges to resident organisms including geologically bounded isolation, no light, variable water flow, and reduced availability of carbon, other nutrients, and oxygen [6,7]. Recent stygobiont research has focused on the ecology of shallow groundwater environments, noting the variable influence of many factors on spatial distribution, including bedrock geology, soil permeability, water chemistry and quality, groundwater levels, adjacent surface flows, riparian vegetation, and climate [8-11]. A recent study documented the role of methane in subterranean food webs [7]. Previous genetic studies identified widespread, longterm barriers to dispersal by groundwater species, even within drainages, despite potentially linking floods [12-15].
Waterbird-Mediated Dispersal and Freshwater Biodiversity: General Insights From Bryozoans
Frontiers in Ecology and Evolution, 2019
Freshwater environments are fragmented and heterogeneous in space and time. Long term persistence thus necessitates at least occasional dispersal of aquatic organisms to locate suitable habitats. However, the insubstantial movements of many require zoochory-hitchhiking a ride with more mobile animals. We review evidence for waterbird-mediated zoochory of freshwater bryozoans, a group that provides an excellent model for addressing this issue. The feasibility of long distance transport by waterbirds of bryozoan propagules (statoblasts) is evaluated in relation to statoblast resistance to extreme conditions and waterbird gut retention times, flight durations and distances. We highlight genetic evidence for colonization following waterbird-mediated transport. The consequences of zoochory for biodiversity are manifold. Taxa that release statoblasts show lower levels of genetic differentiation, genetic divergence and haplotype diversity than those whose statoblasts are retained in situ (hence less available for zoochory). Zoochory may also disseminate pathogens and parasites when infected host stages are transported. Such co-dispersal may explain some disease distributions and is supported by viability of infected statoblasts. Zoochory can also be expected to influence local and regional population and community dynamics, food web structure and stability, and organismal distributions, and abundances. Finally, zoochory may influence host-parasite coevolution and disease dynamics across the landscape with the benefits to parasites depending on their life history (e.g., simple vs. complex life cycles, generalists vs. specialists). Our synthesis highlights the complex ecological and evolutionary impacts of zoochory of freshwater organisms and raises questions for future research.
Diversity and Distributions, 2005
Although Darwin pioneered the study of long-distance dispersal (LDD) of aquatic invertebrates via waterbirds, it remains in its infancy as a modern discipline. A handful of recent studies have quantified internal or external transport in the field, confirming that a variety of long-distance migrants carry invertebrates both internally and externally. These studies show that variation in the morphology of vectors influences the frequency and size of propagules transported, and suggest that more invertebrate groups disperse via birds than was previously thought. Dispersal limitation has mainly been investigated for zooplankton in small experimental systems from which waterbirds were effectively excluded, and the extent of such limitation for invertebrate populations in wetlands interconnected by waterbird movements remains unclear. We expect that the spatial and temporal scales at which dispersal limitation constrains geographical ranges, species richness and genetic structure of invertebrates depends partly on the density of migratory birds using the area. Birds may have a major role in the expansion of exotic species. We propose several avenues for future research. There is a particular need for more quantitative studies of LDD by birds that will enable modellers to assess its role in maintaining invertebrate biodiversity among increasingly fragmented wetlands and in the face of climate change, as well as in the spread of invasive species.
Freshwater Biology, 2023
1. We review progress in our understanding of the importance of waterbirds as dispersal vectors of other organisms, and identify priorities for further research. 2. Waterbirds are excellent for long-distance dispersal (LDD), while other vectors such as fish and mammals disperse similar propagules, but over shorter distances. Empirical studies of internal and external transport by waterbirds have shown that the former mechanism is generally more important. Internal transport is widely recognized for aquatic plants and aquatic invertebrates with resting eggs, but is also important for other organisms (e.g. terrestrial flowering plants not dispersed by frugivores, bryophytes, tardigrades, fish eggs). 3. Waterbird vectors are also important in terrestrial habitats, and provide connectivity across terrestrial-aquatic boundaries. There are important differences in the roles of different waterbird species, especially those using different habitats along the aquatic-terrestrial gradient. Early attempts to predict zoochory based on propagule morphology have been found wanting, and more research is needed into how the traits of vectors and vectored organisms (including life-history, dormancy and growth traits) explain dispersal interactions. Experimental studies have focused on the potential of propagules to survive internal or external transport, and research into factors determining the establishment success of propagules after dispersal is lacking. 4. Recent spatially explicit models of seed dispersal by waterbirds should be expanded to include invertebrate dispersal, and to compare multiple bird species in the same landscape. Network approaches have been applied to plant-waterbird dispersal interactions, and these are needed for invertebrates. Genetic studies support effective LDD of plants and invertebrates along waterbird flyways, but there remains a lack of examples at a local scale. Next Generation Sequencing and genomics should be applied to waterbird-mediated dispersal across the landscape. More studies of biogeography, community ecology, or population genetics should integrate waterbird movements at the design stage. 5. Zoochory research has paid little attention to the dispersal of non-pathogenic microbes (both eukaryotic and prokaryotic). Nevertheless, there is evidence that dispersal via avian guts can be central to the connectivity of aquatic microbial metacommunities. More work on microbial dispersal by waterbirds should explore its implications for biogeochemistry, and the interchange with gut flora of other aquatic organisms. In the Anthropocene, the role of migratory waterbirds in LDD of plants and other organisms is particularly important, e.g. compensating for loss of large migratory mammals and fish, allowing native species to adjust their distributions under global heating, and spreading alien species along flyways after their initial introductions by human vectors. Recent technological advances have opened exciting opportunities that should be fully exploited to further our understanding of dispersal by waterbirds.
Dispersal, Gene Flow, and Population Structure
The Quarterly Review of Biology, 1999
The accuracy ofgenejlozo estinzates is unknown in most natural popzllations becazise direct estimates of dispersal are often not possible. These estimates can be highly imprecise or men biased becazlsepopulation genetic structzlre rejlects more than a simple balance between genetic drft and gene Pow. Most of the models used to estimate gene flow also asszln7e very simple patterns o j movement. As a result, mu1tii)le interpretations of population structure involving contemporary genejlozu, departzlresfrom equilibrium, and otherfactors are almost alwajs possible. One waj to isolate the relative contribution of gene j7ow to lopulation genetic differentiation is to utilize comparative methods. Popzilation genetic statistics szich as F,,, heterozygosity and Areii D can be comfiared between species with d~fmingdis~ersal abilities ifthese species are otizemisephylogeneti-ca10, geopaphicallq' and demopaphicallq' comparable. Accordingb, the available literatzire was searched for all grozips that meet these criteria to determine whether liroad conclzisions regarding the relationships between dispersal, popz~lation genetic structure, and gene flow estimates are posrible. Allozjme and mtDNA data were szimmarizedfor 27 animal grozips i n which dispersal differences can be characterized. I n total, genetic data were obtained for 333 species of vertehrcites and inverlehrates from terrestrial, freshwater and marine habitats. Across these groups, dispersal ability was consistenth related to population structure, with a mean ranlt correlation o f-0.72 between ranlted dispersal ability and F\i. Gene flow estimates derived from private alleles were also cor~elated with dispersal ability, but were less zuideh available. Direct-cozint Izeterozygositj and average values ofNei i D showed moderate de,yrees of correlation with disfiersal ability. Thus, .-despite regzonal, taxonomic and methodological dz3fmnces among tizepoups ofspecies szlr-uejed, available data demonstrate that dispersal makes a measurable contribzition to population qenetic .-A dqferentiation i n the majority of animal species i n natzire, and that genej7ow estimates are rare0 so overwhelmed by population histoq, depaitures from eqziilibjium, or other nzicroevolzitio~zary forces as to be uninformative. A CENTFLU challenge for organismal differ genetically (hereafter referred to as the biologists is to establish links between the level of population genetic differentiation). ecology and the evolution of species. One This is because an in-depth understanding of such link is provided by quantifying the rela-microevolution requires a quantification of tionship between dispersal ability and the mag-how the movement of genes among populanitude and spatial scale over which populations tions (i.e., gene flow) interacts with genetic
Migratory strategies of waterbirds shape the continental-scale dispersal of aquatic organisms
Ecography, 2013
Long distance dispersal (LDD) of propagules is an important determinant of population dynamics, community structuring and biodiversity distribution at landscape, and sometimes continental, scale. Although migratory animals are potential LDD vectors, migratory movement data have never been integrated in estimates of propagule dispersal distances and LDD probability. Here we integrated migratory movement data of two waterbird species (mallard and teal) over two continents (Europe and North America) and gut retention time of different propagules to build a simple mechanistic model of passive dispersal of aquatic plants and zooplankton. Distance and frequency of migratory movements differed both between waterbird species and continents, which in turn resulted in changes in the shapes of propagule dispersal curves. Dispersal distances and the frequency of LDD events (generated by migratory movements) were mainly determined by the disperser species and, to a lesser extent, by the continent. The gut retention time of propagules also exerted a significant effect, which was mediated by the propagule characteristics (e.g. seeds were dispersed farther than Artemia cysts). All estimated dispersal curves were skewed towards local-scale dispersal and, although dispersal distances were lower than previous estimates based only on the vector flight speed, had fat tails produced by LDD events that ranged from 230 to 1209 km. Our results suggest that propagule dispersal curves are determined by the migratory strategy of the disperser species, the region (or flyway) through which the disperser population moves, and the propagule characteristics. Waterbirds in particular may frequently link wetlands separated by hundreds of kilometres, contributing to the maintenance of biodiversity and, given the large geographic scale of the dispersal events, to the readjustment of species distributions in the face of climate change.
Population genetic structure reveals terrestrial affinities for a headwater stream insect
Freshwater Biology, 2007
1. The spatial distribution of stream-dwelling organisms is often considered to be limited primarily according to the hierarchical structure of the hydrologic network, and previous conceptual models of population genetic structure have reflected this generality. Headwater specialists, however, are confined to short upstream sections of the network, and therefore are unlikely to respond in the same way as species with a broader range of habitat tolerance. 2. Here, we propose a model to describe spatial patterns of genetic diversity in headwater specialists with a limited ability for among-stream dispersal. The headwater model predicts a partitioning of genetic variance according to higher-elevation 'islands' of terrestrial habitat that provide required headwater stream conditions. The model therefore expects a geographic pattern of genetic variance similar to that expected for low-dispersal terrestrial species occupying the adjacent habitat. 3. Using a 1032-bp mitochondrial DNA fragment encompassing parts of the COI and COII genes, we demonstrate that Madrean Sky Islands populations of the giant water bug Abedus herberti conform to the proposed headwater model. Furthermore, they exhibit phylogeographic patterns broadly concordant with those shown for several terrestrial species in the region, including a major zone of discontinuity in the Chiricahua mountain range. 4. Overall, populations are highly isolated from one another, and a nested clade analysis suggested that A. herberti population structure, similarly to terrestrial Sky Islands species studied previously, has been influenced by Pleistocene climatic cycles causing expansion and contraction of temperate woodland habitat. 5. Because they have no ability to disperse among present-day mountaintop habitat islands, A. herberti and other headwater species with limited dispersal ability are vulnerable to the projected increasing rate of climatic warming in this region.