Reconstructing the lionfish invasion: insights into Greater Caribbean biogeography

Aim Lionfish (Pterois volitans and P. miles) are popular ornamental fishes native to the Indo‐Pacific that were introduced into Florida waters and are rapidly spreading and establishing throughout the Western Atlantic (WA). Although unfortunate, this invasion provides an excellent system in which to test hypotheses on conservation biology and marine biogeography. The goals of this study are: (1) to document the geographical extent of P. volitans and P. miles; (2) to determine whether the progression of the lionfish invasion is the result of expansion following the initial introduction event or the consequence of multiple introductions at various WA locations; and (3) to analyse the chronology of the invasion in conjunction with the genetic data in order to provide real‐time assessments of hypotheses of marine biogeography. Location The Greater Caribbean, including the US east coast, Bermuda, the Bahamas and the Caribbean Sea. Methods Mitochondrial control region sequences were obtained from lionfish individuals collected from Bermuda and three Caribbean locations and analysed in conjunction with previously published data from five native and two non‐native locations (US east coast and the Bahamas; a total of six WA locations). Genetic variation within and among groups was quantified, and population structure inferred via spatial analyses of molecular variance, pairwise Φ_ST, exact tests, Mantel tests and haplotype networks. Results Mitochondrial DNA screening of WA lionfish shows that while P. miles is restricted to the northernmost locations (Bermuda and the US east coast), P. volitans is ubiquitous and much more abundant. Invasive populations of P. miles and P. volitans have significantly lower levels of genetic diversity relative to their native counterparts, confirming that their introduction resulted in a strong founder effect. Despite the relative genetic homogeneity across the six WA locations, population structure analyses of P. volitans indicate significant differentiation between the northern (US east coast, the Bahamas and Bermuda) and the Caribbean populations. Main conclusions Our findings suggest that the ubiquity of WA lionfish is the result of dispersal from a single source of introduction in Florida and not of multiple independent introductions across the range. In addition, the progression of the lionfish invasion (as documented from sightings), integrated with the genetic evidence, provides support for five of six major scenarios of connectivity and phylogeographical breaks previously inferred for Caribbean organisms.     

Population genomics of rapidly invading lionfish in the Caribbean reveals signals of range expansion in the absence of spatial population structure

Range expansions driven by global change and species invasions may have significant genomic, evolutionary, and ecological implications. During range expansions, strong genetic drift characterized by repeated founder events can result in decreased genetic diversity with increased distance from the center of the historic range, or the point of invasion. The invasion of the Indo‐Pacific lionfish, Pterois volitans, into waters off the US East Coast, Gulf of Mexico, and Caribbean Sea provides a natural system to study rapid range expansion in an invasive marine fish with high dispersal capabilities. We report results from 12,759 single nucleotide polymorphism loci sequenced by restriction enzyme‐associated DNA sequencing for nine P. volitans sampling areas in the invaded range, including Florida and other sites throughout the Caribbean, as well as mitochondrial control region D‐loop data. Analyses revealed low to no spatially explicit metapopulation genetic structure, which is partly consistent with previous finding of little structure within ocean basins, but partly divergent from initial reports of between‐basin structure. Genetic diversity, however, was not homogeneous across all sampled sites. Patterns of genetic diversity correlate with invasion pathway. Observed heterozygosity, averaged across all loci within a population, decreases with distance from Florida while expected heterozygosity is mostly constant in sampled populations, indicating population genetic disequilibrium correlated with distance from the point of invasion. Using an F_ST outlier analysis and a Bayesian environmental correlation analysis, we identified 256 and 616 loci, respectively, that could be experiencing selection or genetic drift. Of these, 24 loci were shared between the two methods.     

Genetic discontinuity among regional populations of <Emphasis Type="Italic">Lophelia pertusa</Emphasis> in the North Atlantic Ocean

Knowledge of the degree to which populations are connected through larval dispersal is imperative to effective management, yet little is known about larval dispersal ability or population connectivity in Lophelia pertusa, the dominant framework-forming coral on the continental slope in the North Atlantic Ocean. Using nine microsatellite DNA markers, we assessed the spatial scale and pattern of genetic connectivity across a large portion of the range of L. pertusa in the North Atlantic Ocean. A Bayesian modeling approach found four distinct genetic groupings corresponding to ocean regions: Gulf of Mexico, coastal southeastern U.S., New England Seamounts, and eastern North Atlantic Ocean. An isolation-by-distance pattern was supported across the study area. Estimates of pairwise population differentiation were greatest with the deepest populations, the New England Seamounts (average F _ST = 0.156). Differentiation was intermediate with the eastern North Atlantic populations (F _ST = 0.085), and smallest between southeastern U.S. and Gulf of Mexico populations (F _ST = 0.019), with evidence of admixture off the southeastern Florida peninsula. Connectivity across larger geographic distances within regions suggests that some larvae are broadly dispersed. Heterozygote deficiencies were detected within the majority of localities suggesting deviation from random mating. Gene flow between ocean regions appears restricted, thus, the most effective management scheme for L. pertusa involves regional reserve networks.     

Genetic structure of the Painted Bunting and its implications for conservation of migratory populations

The Painted Bunting Passerina ciris is a Neotropical songbird which breeds primarily in the USA during the summer and migrates to Mexico, Central America, southern Florida and the Caribbean over the winter. Male Painted Buntings are brightly coloured, which makes them highly sought after as pets, particularly in Mexico, Central America and Europe. We used short sequence repeats (microsatellite DNA) to investigate the population genetic structure of the Painted Bunting and its implications in conservation management of migratory populations. We found a detectable level of population differentiation as revealed by pairwise F_ST and R_ST comparisons and Bayesian clustering analyses, with strong support for differentiation between eastern and western Painted Buntings (e.g. Oklahoma and Georgia F_ST = 0.1; P = 0.005; R_ST = 0.18; P = 0.04) in accordance with previous mitochondrial DNA analysis. We recovered additional support for two sub‐groups within the western clade. While linking migrant songbirds captured outside of the USA to their breeding populations remains a challenge, we show that natural levels of population genetic differentiation can be detected via microsatellite DNA markers and exploited in migratory connectivity studies. We also demonstrate the potential utility of our low‐cost markers for population identification of birds recovered from the pet trade by screening a small subset of samples (n = 5) collected as part of wildlife tracking. We discuss the implications of our results for future efforts to understand patterns of population decline in Painted Buntings more generally, as well as how we might expand this methodology to combat illegal pet‐trade activity in this and other songbird species.     

Population structure and connectivity of the mountainous star coral,Orbicella faveolata,throughout the wider Caribbean region

As coral reefs continue to decline worldwide, it becomes ever more necessary to understand the connectivity between coral populations to develop efficient management strategies facilitating survival and adaptation of coral reefs in the future. Orbicella faveolata is one of the most important reef‐building corals in the Caribbean and has recently experienced severe population reductions. Here, we utilize a panel of nine microsatellite loci to evaluate the genetic structure of O. faveolata and to infer connectivity across ten sites spanning the wider Caribbean region. Populations are generally well‐mixed throughout the basin (F_ST = 0.038), although notable patterns of substructure arise at local and regional scales. Eastern and western populations appear segregated with a genetic break around the Mona Passage in the north, as has been shown previously in other species; however, we find evidence for significant connectivity between Curaçao and Mexico, suggesting that the southern margin of this barrier is permeable to dispersal. Our results also identify a strong genetic break within the Mesoamerican Barrier Reef System associated with complex oceanographic patterns that promote larval retention in southern Belize. Additionally, the diverse genetic signature at Flower Garden Banks suggests its possible function as a downstream genetic sink. The findings reported here are relevant to the ongoing conservation efforts for this important and threatened species, and contribute to the growing understanding of large‐scale coral reef connectivity throughout the wider Caribbean.     

Indo-Pacific lionfish are larger and more abundant on invaded reefs: a comparison of Kenyan and Bahamian lionfish populations

The invasion by Indo-Pacific lionfish (Pterois volitans and P. miles) of the western Atlantic, Caribbean and Gulf of Mexico is emerging as a major threat to coral reef communities across the region. Comparing native and introduced populations of invasive species can reveal shifts in ecology and behaviour that can accompany successful invasions. Using standardized field surveys replicated at multiple sites in Kenya and the Bahamas, we present the first direct comparisons of lionfish density, body size, biomass and behaviour between native and invaded coral reefs. We found that lionfish occur at higher densities with larger body sizes and total biomass on invaded Bahamian coral reefs than the ecologically equivalent species (P. miles) does on native Kenyan reefs. However, the combined average density of the five lionfish species (Pterois miles, P. antennata, P. radiata, Dendrochirus brachypterus and D. zebra) on Kenyan reefs was similar to the density of invasive lionfish in the Bahamas. Understanding the ecological processes that drive these differences can help inform the management and control of invasive lionfish.     

Genetic diversity of the black mangrove (Avicennia germinans L.) in Colombia

This study analyzed the genetic diversity and patterns of genetic structure in Colombian populations of Avicennia germinans L. using microsatellite loci. A lower genetic diversity was found on both the Caribbean (Ho = 0.439) and the Pacific coasts (Ho = 0.277) than reported for the same species in other locations of Central American Pacific, suggesting the deterioration of genetic diversity. All the populations showed high inbreeding coefficients (0.131–0.462) indicating heterozygotes deficience. The genetic structure between the Colombian coasts separated by Central American Isthmus was high (F_RT = 0.39) and the analyses of the genetic patterns of A. germinans revealed a clear differentiation of populations and no-recent gene flow evidence between coasts. Genetic structure was found within each coast (F_ST = 0.10 for the Caribbean coast and F_ST = 0.22 for the Pacific coast). The genetic patterns along the two coasts appear to reflect a forcing by local geomorphology and marine currents. Both coasts constitute a different Evolutionary Significant Unit, so we suggest for future transplantations plans that propagules or saplings of the populations of the Caribbean coast should not be mixed with those of the Pacific Colombian coast. Besides, we suggest that reforestation efforts should carefully distinguish propagules sources within each coast.     

Length‐weight and length‐length relationships of the invasive red lionfish [Pterois volitans (Linnaeus, 1758): Scorpaenidae] in the Parque Nacional Arrecife Alacranes,Southern Gulf of Mexico

Described are the length–weight (LW) and length–length (LL) relationships of the Indo–Pacific, red lionfish [Pterois volitans (Linnaeus, 1758): Scorpaenidae] – an invasive fish introduced into the coral reefs of the Western Atlantic. Volunteer diver‐fishers speared a total of 455 red lionfish (range 9–35 cm TL) from July 2010 to December 2011 in the Parque Nacional Arrecife Alacranes, off the northern coast of the Yucatan Peninsula, Mexico. The LWR obtained in the combined data was W = 0.104TL^3.309.     

Seascape continuity plays an important role in determining patterns of spatial genetic structure in a coral reef fish

Detecting patterns of spatial genetic structure (SGS) can help identify intrinsic and extrinsic barriers to gene flow within metapopulations. For marine organisms such as coral reef fishes, identifying these barriers is critical to predicting evolutionary dynamics and demarcating evolutionarily significant units for conservation. In this study, we adopted an alternative hypothesis‐testing framework to identify the patterns and predictors of SGS in the Caribbean reef fish Elacatinus lori. First, genetic structure was estimated using nuclear microsatellites and mitochondrial cytochrome b sequences. Next, clustering and network analyses were applied to visualize patterns of SGS. Finally, logistic regressions and linear mixed models were used to identify the predictors of SGS. Both sets of markers revealed low global structure: mitochondrial Φ_ST = 0.12, microsatellite F_ST = 0.0056. However, there was high variability among pairwise estimates, ranging from no differentiation between sites on contiguous reef (Φ_ST = 0) to strong differentiation between sites separated by ocean expanses ≥ 20 km (maximum Φ_ST = 0.65). Genetic clustering and statistical analyses provided additional support for the hypothesis that seascape discontinuity, represented by oceanic breaks between patches of reef habitat, is a key predictor of SGS in E. lori. Notably, the estimated patterns and predictors of SGS were consistent between both sets of markers. Combined with previous studies of dispersal in E. lori, these results suggest that the interaction between seascape continuity and the dispersal kernel plays an important role in determining genetic connectivity within metapopulations.     

Evidence of two genetic clusters of manatees with low genetic diversity in Mexico and implications for their conservation

The Antillean manatee (Trichechus manatus manatus) occupies the tropical coastal waters of the Greater Antilles and Caribbean, extending from Mexico along Central and South America to Brazil. Historically, manatees were abundant in Mexico, but hunting during the pre-Columbian period, the Spanish colonization and throughout the history of Mexico, has resulted in the significantly reduced population occupying Mexico today. The genetic structure, using microsatellites, shows the presence of two populations in Mexico: the Gulf of Mexico (GMx) and Chetumal Bay (ChB) on the Caribbean coast, with a zone of admixture in between. Both populations show low genetic diversity (GMx: N_A = 2.69; H_E = 0.41 and ChB: N_A = 3.0; H_E = 0.46). The lower genetic diversity found in the GMx, the largest manatee population in Mexico, is probably due to a combination of a founder effect, as this is the northern range of the sub-species of T. m. manatus, and a bottleneck event. The greater genetic diversity observed along the Caribbean coast, which also has the smallest estimated number of individuals, is possibly due to manatees that come from the GMx and Belize. There is evidence to support limited or unidirectional gene flow between these two important areas. The analyses presented here also suggest minimal evidence of a handful of individual migrants possibly between Florida and Mexico. To address management issues we suggest considering two distinct genetic populations in Mexico, one along the Caribbean coast and one in the riverine systems connected to the GMx.     

Biophysical connectivity explains population genetic structure in a highly dispersive marine species

Connectivity, the exchange of individuals among locations, is a fundamental ecological process that explains how otherwise disparate populations interact. For most marine organisms, dispersal occurs primarily during a pelagic larval phase that connects populations. We paired population structure from comprehensive genetic sampling and biophysical larval transport modeling to describe how spiny lobster (Panulirus argus) population differentiation is related to biological oceanography. A total of 581 lobsters were genotyped with 11 microsatellites from ten locations around the greater Caribbean. The overall F _ST of 0.0016 (P = 0.005) suggested low yet significant levels of structuring among sites. An isolation by geographic distance model did not explain spatial patterns of genetic differentiation in P. argus (P = 0.19; Mantel r = 0.18), whereas a biophysical connectivity model provided a significant explanation of population differentiation (P = 0.04; Mantel r = 0.47). Thus, even for a widely dispersing species, dispersal occurs over a continuum where basin-wide larval retention creates genetic structure. Our study provides a framework for future explorations of wide-scale larval dispersal and marine connectivity by integrating empirical genetic research and probabilistic modeling.

     

Allelopathy in the tropical alga Lobophora variegata (Phaeophyceae): mechanistic basis for a phase shift on mesophotic coral reefs?

Macroalgal phase shifts on Caribbean reefs have been reported with increasing frequency, and recent reports of these changes on mesophotic coral reefs have raised questions regarding the mechanistic processes behind algal population expansions to deeper depths. The brown alga Lobophora variegata is a dominant species on many shallow and deep coral reefs of the Caribbean and Pacific, and it increased in percent cover (>50%) up to 61 m on Bahamian reefs following the invasion of the lionfish Pterois volitans. We examined the physiological and ecological constraints contributing to the spread of Lobophora on Bahamian reefs across a mesophotic depth gradient from 30 to 61 m, pre‐ and post‐lionfish invasion. Results indicate that there were no physiological limitations to the depth distribution of Lobophora within this range prior to the lionfish invasion. Herbivory by acanthurids and scarids in algal recruitment plots at mesophotic depths was higher prior to the lionfish invasion, and Lobophora chemical defenses were ineffective against an omnivorous fish species. In contrast, Lobophora exhibited significant allelopathic activity against the coral Montastraea cavernosa and the sponge Agelas clathrodes in laboratory assays. These data indicate that when lionfish predation on herbivorous fish released Lobophora from grazing pressure at depth, Lobophora expanded its benthic cover to a depth of 61 m, where it replaced the dominant coral and sponge species. Our results suggest that this chemically defended alga may out‐compete these species in situ, and that mesophotic reefs may be further impacted in the near future as Lobophora continues to expand to its compensation point.     

Phase shift to algal dominated communities at mesophotic depths associated with lionfish (<Emphasis Type="Italic">Pterois volitans</Emphasis>) invasion on a Bahamian coral reef

Mesophotic coral reefs (30–150 m) have been assumed to be physically and biologically connected to their shallow-water counterparts, and thus may serve as refugia for important taxonomic groups such as corals, sponges, and fish. The recent invasion of the Indo–Pacific lionfish (Pterois volitans) onto shallow reefs of the Caribbean and Bahamas has had significant, negative, effects on shallow coral reef fish populations. In the Bahamas, lionfish have extended their habitat range into mesophotic depths down to 91 m where they have reduced the diversity of several important fish guilds, including herbivores. A phase shift to an algal dominated (>50% benthic cover) community occurred simultaneously with the loss of herbivores to a depth of 61 m and caused a significant decline in corals and sponges at mesophotic depths. The effects of this invasive lionfish on mesophotic coral reefs and the subsequent changes in benthic community structure could not be explained by coral bleaching, overfishing, hurricanes, or disease independently or in combination. The significant ecological effects of the lionfish invasion into mesophotic depths of coral reefs casts doubt on whether these communities have the resilience to recover themselves or contribute to the recovery of their shallow water counterparts as refugia for key coral reef taxa.     

Genetic diversity of Lavandula multifida L. (Lamiaceae) in Tunisia: implication for conservation

The genetic variation within and among eight Tunisian natural populations of Lavandula multifida L., from different bioclimatic zones was assessed using random amplified polymorphic DNA (RAPDs). Of a total of 97 generated bands from seven selected primers, 84 bands were polymorphic. The genetic diversity within a population was high and varied according to the populations (0.308 < H’ < 0.459) without relationships to altitudes or pluviothermic indices of sites. The genetic differentiation among populations was high (G_ST = 0.395 and Φ_ST = 0.318). All population pairs were significantly differentiated. Among populations, within ecological groups genetic structure was high (0.219); whilst among them it was low (Φ_CT = 0.049; P < 0.05). The correlation between Φ_ST and geographic distance matrices among pairs of populations was not significant, suggesting that genetic connectivity between populations has a stochastic component at all spatial scales. The neighbour‐joining cluster analysis showed that individuals from each population clustered together. UPGMA cluster analysis showed that population groupings are not strictly in accordance with bioclimates or geographic location. The genetic differentiation in L. multifida could have occurred at local scales because of genetic drift. Efforts should be made to protect all populations. The maintenance of substantial population size should be initiated via fencing and controlling collection to restore the regeneration of populations.     

High degree of genetic differentiation in marine three‐spined sticklebacks (Gasterosteus aculeatus)

Populations of widespread marine organisms are typically characterized by a low degree of genetic differentiation in neutral genetic markers, but much less is known about differentiation in genes whose functional roles are associated with specific selection regimes. To uncover possible adaptive population divergence and heterogeneous genomic differentiation in marine three‐spined sticklebacks (Gasterosteus aculeatus), we used a candidate gene‐based genome‐scan approach to analyse variability in 138 microsatellite loci located within/close to (<6 kb) functionally important genes in samples collected from ten geographic locations. The degree of genetic differentiation in markers classified as neutral or under balancing selection—as determined with several outlier detection methods—was low (F_ST = 0.033 or 0.011, respectively), whereas average F_ST for directionally selected markers was significantly higher (F_ST = 0.097). Clustering analyses provided support for genomic and geographic heterogeneity in selection: six genetic clusters were identified based on allele frequency differences in the directionally selected loci, whereas four were identified with the neutral loci. Allelic variation in several loci exhibited significant associations with environmental variables, supporting the conjecture that temperature and salinity, but not optic conditions, are important drivers of adaptive divergence among populations. In general, these results suggest that in spite of the high degree of physical connectivity and gene flow as inferred from neutral marker genes, marine stickleback populations are strongly genetically structured in loci associated with functionally relevant genes.     

Evidence for adaptive phenotypic differentiation in Baltic Sea sticklebacks

The evidence for adaptive phenotypic differentiation in mobile marine species remains scarce, partly due to the difficulty of obtaining quantitative genetic data to demonstrate the genetic basis of the observed phenotypic differentiation. Using a combination of phenotypic and molecular genetic approaches, we elucidated the relative roles of natural selection and genetic drift in explaining lateral plate number differentiation in threespine sticklebacks (Gasterosteus aculeatus) across the entire Baltic Sea basin (approximately 392 000 km²). We found that phenotypic differentiation (P_ST = 0.213) in plate number exceeded that in neutral markers (F_ST = 0.008), suggesting an adaptive basis for the observed differentiation. Because a close correspondence was found between plate phenotype and genotype at a quantitative trait loci (QTL; STN381) tightly linked to the gene (Ectodysplasin) underlying plate variation, the evidence for adaptive differentiation was confirmed by comparison of F_ST at the QTL (F_STQ = 0.089) with F_ST at neutral marker loci. Hence, the results provide a comprehensive demonstration of adaptive phenotypic differentiation in a high‐gene‐flow marine environment with direct, rather than inferred, verification for the genetic basis of this differentiation. In general, the results illustrate the utility of P_ST–F_ST–F_STQ comparisons in uncovering footprints of natural selection and evolution and add to the growing evidence for adaptive genetic differentiation in high‐gene‐flow marine environments, including that of the relatively young Baltic Sea.     

High connectivity among argali sheep from Afghanistan and adjacent countries: Inferences from neutral and candidate gene microsatellites

We quantified population connectivity and genetic variation in the Marco Polo subspecies of argali mountain sheep (Ovis ammon polii) by genotyping 9 neutral and 8 candidate gene microsatellite loci in 172 individuals noninvasively sampled across five study areas in Afghanistan, China, and Tajikistan. Heterozygosity and allelic richness were generally high (mean H = 0.67, mean A = 6.1), but were significantly lower in the China study area (H = 0.61, P < 0.001; A = 4.9, P < 0.01). One marker in an immune system gene (TCRG4) showed an excess of rare alleles compared to neutral expectations. Another immune system gene (GLYCAM-1) showed excessive differentiation (high F _ST) between study areas. Estimates of genetic differentiation were similar (F _ST = 0.035 vs. 0.033) with and without the two loci deviating from neutrality, suggesting that selection is not a primary driver of overall molecular variation, and that candidate gene loci can be used for connectivity monitoring, as long as selection tests are conducted to avoid biased gene flow estimates. Adequate protection of argali and maintenance of inter-population connectivity will require monitoring and international cooperation because argali exhibit high gene flow across international borders.     

Selection on life‐history traits and genetic population divergence in rotifers

A combination of founder effects and local adaptation – the Monopolization hypothesis – has been proposed to reconcile the strong population differentiation of zooplankton dwelling in ponds and lakes and their high dispersal abilities. The role genetic drift plays in genetic differentiation of zooplankton is well documented, but the impact of natural selection has received less attention. Here, we compare differentiation in neutral genetic markers (F_ST) and in quantitative traits (Q_ST) in six natural populations of the rotifer Brachionus plicatilis to assess the importance of natural selection in explaining genetic differentiation of life‐history traits. Five life‐history traits were measured in four temperature × salinity combinations in common‐garden experiments. Population differentiation for neutral genetic markers – 11 microsatellite loci – was very high (F_ST = 0.482). Differentiation in life‐history traits was higher in traits related to sexual reproduction than in those related to asexual reproduction. Q_ST values for diapausing egg production (a trait related to sexual reproduction) were higher than their corresponding F_ST in some pairs of populations. Our results indicate the importance of divergent natural selection in these populations and suggest local adaptation to the unpredictability of B. plicatilis habitats.