Genetic signatures of translocations and habitat fragmentation for two evolutionarily significant units of a protected fish species

Genetic population structure was evaluated for the White Sands pupfish (Cyprinodon tularosa), a protected fish species comprised of two Evolutionarily Significant Units (ESUs); the Malpais Spring ESU and the Salt Creek ESU. The Malpais Spring ESU is restricted to Malpais Spring, whereas the Salt Creek ESU includes the native Salt Creek population and two Salt Creek-derived populations at Mound Spring and Lost River; all three of these habitats are physically fragmented. We sampled the upper and lower reaches of the four populations, examining 13 DNA microsatellite loci from 40 individuals per population. As expected, significant genetic structure was observed between the two ESUs; Malpais Spring and Salt Creek. Substantial genetic drift was observed for the introduced Lost River population, with modest genetic drift for the introduced Mound Spring population. Taken together with ecological data, neither of the introduced populations successfully replicates the Salt Creek population. We also report significant reductions in genetic diversity for the upper reaches of both Salt Creek and Lost River, indicating that recent habitat changes have altered the genetic structure of these two populations. We consider these findings along with previously reported ecological data to develop guidelines for managing C. tularosa.     

线粒体DNA（mtDNA）多态性在动物保护生物学中的应用

本文从两个方面论述了mtDNA在动物保护生物学中的应用：一是对物种进行遗传多样性的检 测与管理,二是进行与种群统计学数据相关的遗传分析。前者与保护的长期效益（如进化） 密切相关,而后者则主要用于指导短期管理措施的制定。同时,本文重点论述了mtDNA在进 化显著单位(ESUs)和管理单位(MUs)的认定方面的作用。认定ESUs的目的是隔离管理遗传多 样性,它是一系列系统进化史独特的种群,这种独特性同时表现在mtDNA和核DNA上;MUs是 种群统计意义上的生殖隔离单位,具有独特的等位基因频率,与系统发生结构和遗传分歧水 平无关。ESUs与MUs都是保护生物学中保护与管理的重要基本单位。     

Highly local environmental variability promotes intrapopulation divergence of quantitative traits: an example from tropical rain forest trees

Background and Aims

In habitat mosaics, plant populations face environmental heterogeneity over short geographical distances. Such steep environmental gradients can induce ecological divergence. Lowland rainforests of the Guiana Shield are characterized by sharp, short-distance environmental variations related to topography and soil characteristics (from waterlogged bottomlands on hydromorphic soils to well-drained terra firme on ferralitic soils). Continuous plant populations distributed along such gradients are an interesting system to study intrapopulation divergence at highly local scales. This study tested (1) whether conspecific populations growing in different habitats diverge at functional traits, and (2) whether they diverge in the same way as congeneric species having different habitat preferences.

Methods

Phenotypic differentiation was studied within continuous populations occupying different habitats for two congeneric, sympatric, and ecologically divergent tree species (Eperua falcata and E. grandiflora, Fabaceae). Over 3000 seeds collected from three habitats were germinated and grown in a common garden experiment, and 23 morphological, biomass, resource allocation and physiological traits were measured.

Key Results

In both species, seedling populations native of different habitats displayed phenotypic divergence for several traits (including seedling growth, biomass allocation, leaf chemistry, photosynthesis and carbon isotope composition). This may occur through heritable genetic variation or other maternally inherited effects. For a sub-set of traits, the intraspecific divergence associated with environmental variation coincided with interspecific divergence.

Conclusions

The results indicate that mother trees from different habitats transmit divergent trait values to their progeny, and suggest that local environmental variation selects for different trait optima even at a very local spatial scale. Traits for which differentiation within species follows the same pattern as differentiation between species indicate that the same ecological processes underlie intra- and interspecific variation.     

Identifying evolutionarily significant units for conservation of the endangered Malus sieversii using genome‐wide RADseq data

Malus sieversii, a wild progenitor of the domesticated apple, is an endangered species and is assigned second conservation priority by the China Plant Red Data Book. It is urgent to carry out in situ conservation of this species, but previous studies have not identified evolutionarily significant units (ESUs) for conservation management. In this study, we investigated the genetic diversity and relationships of six M. sieversii populations from China using integrated analysis of microsatellite (nSSR) data, genome‐wide SNPs and previous results in order to propose a reasonable conservation management. The results showed that levels of genetic diversity were inconsistently reflected by our nSSR and previous studies, suggesting that indices of genetic diversity are not effective to identify priority conservation areas for M. sieversii. Based on the selection criteria of ESUs for endangered species conservation, ESUs should reflect lineage divergence, geographical separation and different adaptive variation. Our phylogenetic tree based on genome‐wide SNPs yielded a clear relationship of divergent lineages among M. sieversii populations, leading to new different from those of previous studies. Three independent lineages, including the pairs of populations Huocheng‐Yining, Gongliu‐Xinyuan and Tuoli‐Emin, were identified. The geographic distances between populations among the different phylogenetic lineages were much greater than those within the same phylogenetic lineage. A cluster analysis on environmental variables showed that the three independent lineages inhabit different environmental conditions, suggesting that they may have adapted to different environments. Based on the results, we propose that three independent ESUs should be recognized as conservation units for M. sieversii in China.     

Common Garden Experiment Reveals Genetic Control of Phenotypic Divergence between Swamp Sparrow Subspecies That Lack Divergence in Neutral Genotypes

Background

Adaptive divergence between populations in the face of strong selection on key traits can lead to morphological divergence between populations without concomitant divergence in neutral DNA. Thus, the practice of identifying genetically distinct populations based on divergence in neutral DNA may lead to a taxonomy that ignores evolutionarily important, rapidly evolving, locally-adapted populations. Providing evidence for a genetic basis of morphological divergence between rapidly evolving populations that lack divergence in selectively neutral DNA will not only inform conservation efforts but also provide insight into the mechanisms of the early processes of speciation. The coastal plain swamp sparrow, a recent colonist of tidal marsh habitat, differs from conspecific populations in a variety of phenotypic traits yet remains undifferentiated in neutral DNA.

Methods and Principal Findings

Here we use an experimental approach to demonstrate that phenotypic divergence between ecologically separated populations of swamp sparrows is the result of local adaptation despite the lack of divergence in neutral DNA. We find that morphological (bill size and plumage coloration) and life history (reproductive effort) differences observed between wild populations were maintained in laboratory raised individuals suggesting genetic divergence of fitness related traits.

Conclusions and Significance

Our results support the hypothesis that phenotypic divergence in swamps sparrows is the result of genetic differentiation, and demonstrate that adaptive traits have evolved more rapidly than neutral DNA in these ecologically divergent populations that may be in the early stages of speciation. Thus, identifying evolutionarily important populations based on divergence in selectively neutral DNA could miss an important level of biodiversity and mislead conservation efforts.     

Using microsatellite and MHC variation to identify species, ESUs, and MUs in the endangered Sonoran topminnow

Highly variable loci can provide insight into the recognition of species, evolutionarily significant units (ESUs) and management units (MUs). In general, the ESU and MU categories are thought to be reflective of adaptive differences between them. Here we examine this premise by presenting a comprehensive examination of genetic variation for both microsatellite loci and a major histocompatibility complex (MHC) locus, thought to be of adaptive significance, in the endangered Sonoran topminnow. The extent of variation for the microsatellite loci and the MHC gene within the 13 populations of the Gila topminnow is highly correlated, suggesting that nonselective factors have played an important role in influencing variation within and between populations for the MHC locus. Therefore, using all of these loci, we found that the eight natural populations of the Gila topminnow fell into two different ESUs, one of which had four different MUs. The source of the Boyce Thompson sample, a population that was used extensively for restocking, appeared to be Monkey Spring. The source of the Watson Wash population also appeared to be Monkey Spring (or Boyce Thompson). The newly colonized Santa Cruz River population, which had the most genetic variation of any Gila topminnow population, appeared to descend primarily from Sonoita Creek populations. The Yaqui topminnow, presently considered another subspecies of the Sonoran topminnow, was very distinct for both microsatellite (only two of 25 alleles found in the Yaqui were in any of the Gila topminnow samples) and MHC alleles (nonoverlapping sets of alleles for the two groups). As a result, it appeared that the taxonomic status of the two subspecies should be re-evaluated and that full species status for Gila and Yaqui topminnows was appropriate. There was evidence for the importance of long-term selection at the MHC locus in the higher rate of nonsynonymous than synonymous substitution. In addition, there appeared to have been a duplication of the MHC locus that was present in most of the fish in six of the natural populations of the Gila topminnow.     

Disjunct,highly divergent genetic lineages within two rare Eremophila (Scrophulariaceae: Myoporeae) species in a biodiversity hotspot: implications for taxonomy and conservation

Effective conservation management should target appropriate conservation units, but evolutionarily and genetically divergent lineages within nominal taxa are often unrecognized. The south‐western Australian biodiversity hotspot may harbour many cryptic taxa, as it contains many plant species with naturally fragmented population distributions. Using microsatellite markers, we tested the hypothesis that disjunct population groups in the rare species Eremophila microtheca and E. rostrata (Scrophulariaceae: Myoporeae) are highly genetically divergent and represent separate evolutionarily significant units (ESUs). Chromosome counts indicated that all individuals assessed were diploid (2n = 36). Genetic differentiation among disjunct population groups was highly significant (P < 0.001) for both E. microtheca (F_ST = 0.301–0.383; D_est = 0.756–0.774) and E. rostrata (F_ST = 0.325–0.346; D_est = 0.628–0.660), and was similar to their differentiation from allied species. These results, including high incidences of private alleles, suggest historical divergence among cryptic taxa within E. microtheca and E. rostrata. Population groups in E. rostrata have recently been taxonomically recognized as two subspecies. Our study suggests that E. microtheca should also be reassessed as two taxa or considered as two ESUs, and the southern occurrence should be listed as Critically Endangered. We suggest a precautionary approach for flora in this and similar landscapes, whereby historically wide geographical disjunctions are assumed to indicate separate units for conservation. © 2014 State of Western Australia. Botanical Journal of the Linnean Society © 2014 The Linnean Society of London, 2015, 177 , 96–111.     

Genetic analysis and uncertain taxonomic status of threatened Foskett Spring speckled dace

Foskett Spring is a small isolated desert spring in the Warner Basin of Oregon containing an undescribed subspecies of speckled dace protected under the US Endangered Species Act. Uncertainty regarding the taxonomic status of Foskett dace has raised questions about their evolutionary relationship to other more abundant populations in the Warner Basin. To address these questions, we sequenced 1,982 base pairs (bp) of the ND2 and cyt-b genes of mitochondrial DNA (mtDNA) for 85 fish from Foskett Spring, the surrounding Warner Basin, and the adjacent Goose Lake Basin. We observed 58 unique mtDNA haplotypes defined by 96 bp substitutions in both genes. MtDNA sequences were highly divergent and reciprocally monophyletic between dace from the Warner and Goose Lake Basins, with sequence divergences (5 and 3% at ND2 and cyt-b, respectively) in the range usually observed between fish species. In contrast, mean sequence divergence between Foskett dace and other Warner Basin populations was less than 1%, with no evidence of reciprocal monophyly among mtDNA lineages. These results indicate that Foskett dace and other populations in the Warner Basin are approximately equally diverged from one another evolutionarily, suggesting similar times of divergence since the late Pleistocene. We believe further studies are needed to determine if rapid evolution of novel traits have occurred in dace inhabiting the unique ecological setting of Foskett Spring during the past 10,000 years.     

Phylogeographic structure in the threatened Yarra pygmy perch <Emphasis Type="Italic">Nannoperca obscura</Emphasis> (Teleostei: Percichthyidae) has major implications for declining populations

Molecular genetic information should be a pre-requisite when evaluating conservation priorities in highly structured species such as freshwater fishes. Nuclear (allozyme) and mitochondrial (cytochrome b) markers were used to investigate phylogeographic structure in the Yarra pygmy perch Nannoperca obscura (Klunzinger), a threatened freshwater fish endemic to mainland south-eastern Australia. Complementary patterns of strong, geographically defined sub-structure were observed including a major east–west divergence (at the Glenelg River), four diagnosable lineages, and statistically-significant differences between most populations. Accordingly, four Evolutionarily Significant Units (ESUs) are defined and multiple, drainage-scale Management Units (MUs) suggested. Since Nannoperca obscura is a relatively poor disperser with no apparent gene flow between most populations, any regional extirpation would see the irreversible loss of genetic diversity. This is problematic, as several populations, most notably a recently discovered ESU in the Murray-Darling Basin, are feared extirpated through a combination of anthropogenic threats and severe drought. The potential loss of unique evolutionarily components within N. obscura soon after their discovery highlights with some urgency, the need to define and protect conservation units in highly modified freshwater habitats.     

Creating and destroying species: the 'new' biodiversity and evolutionarily significant units among New Zealand's galaxiid fishes

Morphological and genetic analyses of populations of two non-diadromous galaxiid species, the black mudfish and Neochanna heleios , the dwarf inanga Galaxias gracilis confirm the presence of a cryptic species, Neochanna heleios , within the geographic range of N. diversus , and indicate three distinct evolutionarily significant units (ESUs) in the latter species. Comparisons between G. gracilis and its parent taxon, G. maculatus , reveal that the former is not monophyletic and derives from three separate founding events. Significant morphological divergence between these two species is the result of ontogenic shifts in landlocked lacustrine populations and long-term morphological convergence in populations of G. gracilis. . Corresponding incipient changes are recognized in other younger landlocked populations of G. maculatus in New Zealand. These populations and the three groups within G. gracilis should be given the status of ESUs and managed accordingly by conservation agencies.     

The relative roles of cultural drift and acoustic adaptation in shaping syllable repertoires of island bird populations change with time since colonization

In birds, song divergence often precedes and facilitates divergence of other traits. We assessed the relative roles of cultural drift, innovation, and acoustic adaptation in divergence of island bird dialects, using silvereyes (Zosterops lateralis). In recently colonized populations, syllable diversity was not significantly lower than source populations, shared syllables between populations decreased with increasing number of founder events, and dialect variation displayed contributions from both habitat features and drift. The breadth of multivariate space occupied by recently colonized Z. l. lateralis populations was comparable to evolutionarily old forms that have diverged over thousands to hundreds of thousands of years. In evolutionarily old subspecies, syllable diversity was comparable to the mainland and the amount of variation in syllable composition explained by habitat features increased by two‐ to threefold compared to recently colonized populations. Together these results suggest that cultural drift influences syllable repertoires in recently colonized populations, but innovation likely counters syllable loss from colonization. In evolutionarily older populations, the influence of acoustic adaptation increases, possibly favoring a high diversity of syllables. These results suggest that the relative importance of cultural drift and acoustic adaptation changes with time since colonization in island bird populations, highlighting the value of considering multiple mechanisms and timescale of divergence when investigating island song divergence.     

Phylogeographic evidence links the threatened ‘Grampians’ Mountain Dragon (Rankinia diemensis Grampians) with Tasmanian populations: conservation implications in south-eastern Australia

The importance of protecting genetic diversity within a species is increasingly being recognised by conservation management authorities. However, discrepancies in conservation policy between authorities, such as state versus national bodies, can have significant implications for species management when they cross state boundaries. We conducted a phylogeographic study of the south-eastern Australian lizard Rankinia diemensis to identify evolutionary significant units (ESUs), including the endangered population from the Grampians National Park in western Victoria. Phylogenetic analyses of two gene regions (mtDNA: ND2; nuclear: RAG1) revealed high levels of genetic divergence between populations, indicating isolation over long evolutionary time frames. Based on criteria of genetic divergence and isolation, R. diemensis contains at least two ESUs that require specific management. We found that R. diemensis from the Grampians are closely related to Tasmanian populations, but that the divergence between these regions is great enough (3.7 % mtDNA) that they should be considered separate ESUs. However, we believe the close evolutionary ties between these two regions needs to be taken into account; yet under current practises, conservation management of subspecific ESUs relies on state-level efforts. We argue that another population that occurs on the Victorian coast also qualifies as an ESU and requires targeted conservation action. Rankinia diemensis provides a case-in-point of the discrepancy between the state-level approach of maintaining genetic variation within a species and the more conservative Commonwealth focus on conserving biodiversity at the species level.     

Comparative Phyloclimatic Analysis and Evolution of Ecological Niches in the Scimitar Babblers (Aves: Timaliidae: Pomatorhinus)

We present the first extensive and integrative analysis of niche evolution based on climatic variables and a dated molecular phylogeny of a heterogeneous avian group of Southeast Asian scimitar babblers of the genus Pomatorhinus. The four main clades of scimitar babblers have species that co-occur in similar areas across southern Asia but some have diverged at different timeframes, with the most recently evolved clade harboring the highest number of species. Ecological niche models and analysis of contributing variables within a phylogenetic framework indicate instances of convergent evolution of members of different clades onto similar ecological parameter space, as well as divergent evolution of members from within clades. Pomatorhinus species from different clades occupying Himalayan foothills show convergence towards similar climatic tolerances, whereas within a clade, allopatric sister-species occurring in the Himalayas have diverged to occupy different climatic parameter spaces. Comparisons of climatic tolerances of Himalayan foothills taxa with species distributed further south in Assam/Burma and Burma/Thailand indicate convergence towards similar parameter spaces in several climatic variables. Niche overlap was observed to be lower among species of the youngest clade (ruficollis) and higher among species of older clades (ferruginosus). Analysis of accumulation of ecological disparity through time indicates rapid divergence within recent time frames. As a result, Himalayan taxa originating at different temporal scales within the four main scimitar babbler clades have differentiated ecologically only in recently diverged taxa. Our study suggests that the repeated orogenic and climatic fluctuations of the Pliocene and Pleistocene within mainland Southeast Asia served as an important ecological speciation driver within scimitar babblers, by providing opportunities for rapid geographic expansion and filling of novel environmental niches.     

Simulated climate warming causes asymmetric responses in insect life-history timing potentially disrupting a classic ecological speciation system

Climate change may alter phenology within populations with cascading consequences for community interactions and on-going evolutionary processes. Here, we measured the response to climate warming in two sympatric, recently diverged (~170 years) populations of Rhagoletis pomonella flies specialized on different host fruits (hawthorn and apple) and their parasitoid wasp communities. We tested whether warmer temperatures affect dormancy regulation and its consequences for synchrony across trophic levels and temporal isolation between divergent populations. Under warmer temperatures, both fly populations developed earlier. However, warming significantly increased the proportion of maladaptive pre-winter development in apple, but not hawthorn, flies. Parasitoid phenology was less affected, potentially generating ecological asynchrony. Observed shifts in fly phenology under warming may decrease temporal isolation, potentially limiting on-going divergence. Our findings of complex sensitivity of life-history timing to changing temperatures predict that coming decades may see multifaceted ecological and evolutionary changes in temporal specialist communities.     

Evolutionarily significant units in a flightless ground beetle show different climate niches and high extinction risk due to climate change

Species distribution models (SDMs), especially those basing on climatic parameters, have frequently been used to project future species ranges and to develop conservation strategies. As suggested by several authors, we considered both different dispersal abilities and different evolutionarily significant units (ESUs, as determined in an earlier genetic survey). For our study species, the flightless ground beetle Carabus irregularis, SDMs for two ESUs from the western and the Carpathian area of the distribution range showed immense, and deviating future range contractions reflecting divergent ecological requirements. As minimal dispersal SDMs resulted in a stronger decline of future ranges than the maximal dispersal models, low dispersal ability tended to strengthen the already high vulnerability of the cold-adapted mountain species to global warming. Areas shown in our maximal dispersal models as offering climatically suitable habitats for C. irregularis in the future should be considered as potential areas of action in future conservation planning (e.g. assisted migration or assisted colonisation). Thus, both dispersal scenarios and different (if applicable) ESUs should be considered when developing SDMs as useful tools for species conservation strategies adapted to species’ performance and differentiation patterns.     

Subspecies of the Central American Squirrel Monkey (Saimiri oerstedii) as Units for Conservation

The accurate diagnosis of conservation units now typically includes recognition of genetic diversity and unique evolutionary lineages and is necessary to inform the conservation management of endangered species. We evaluated whether the two currently recognized subspecies of the endangered Central American squirrel monkey (Saimiri oerstedii) in Costa Rica are evolutionarily significant units (ESUs) that should be managed separately in conservation efforts. We used previously published sequences of 50 individuals of Saimiri oerstedii for 880 bp of the mtDNA d-loop and genotypes of 244 individuals for 16 microsatellites and conducted novel analyses to characterize genetic differentiation between subspecies of Saimiri oerstedii. We measured sequence differentiation and inferred an intraspecific molecular phylogeny and a haplotype network, and found consistent results supporting statistically significant divergence and reciprocal monophyly between subspecies. A population aggregation analysis also supported Saimiri oerstedii citrinellus and S. o. oerstedii as diagnosably distinct units. These results confirm previous genetic studies with smaller sample sizes and are consistent with other factors including differences in pelage and morphology and divergence at nuclear markers. Conservation managers should manage these subspecies separately to prevent the loss of genetic diversity via artificially induced outbreeding. High levels of genetic diversity may buffer populations against outside extinction pressures, to which Saimiri oerstedii are vulnerable because of their dwindling habitat and small population size.     

Molecular and morphological assessment of Australia’s most endangered snake, <Emphasis Type="Italic">Hoplocephalus bungaroides</Emphasis>, reveals two evolutionarily significant units for conservation

The Broad-headed snake Hoplocephalus bungaroides is one of Australia’s most endangered vertebrates. Extant populations of H. bungaroides are restricted to several geographically isolated reserves to the north, west, and south of Sydney. We analysed mitochondrial DNA from 184 specimens drawn from across the geographic range of the Broad-headed snake. Phylogenetic analysis demonstrated that H. bungaroides comprises two divergent mitochondrial lineages with a “northern” clade comprising populations west and north of Sydney and a “southern” clade comprising animals in Morton National Park. The two clades differ by an uncorrected genetic distance of 1.7%, which implies a divergence dating to approximately 755,000–850,000 years ago. We complemented our molecular data set with a detailed analysis of morphological variation both between and within the genetic clades. The two H. bungaroides genetic clades are morphologically indistinguishable and show little sexual dimorphism. Our results demonstrate that the populations north and south of this biogeographic split function as two distinct populations with no recent gene flow. There is no reason for separate taxonomic recognition of these two clades, but they do represent distinct evolutionarily significant units (ESUs) that require separate conservation management. In addition, within the northern ESU, populations from Royal National Park, Blue Mountains National Park, Wollemi National Park, and the Sydney Water Catchment supply areas should be considered as separate management units to conserve both evolutionary and ecological processes.     

Identification of evolutionarily significant units in the Cuban endemic damselfly <Emphasis Type="Italic">Hypolestes trinitatis</Emphasis> (Odonata: Hypolestidae)

Species classification may not reflect the underlying/cryptic genetic diversity which should otherwise be conserved as it represents the potential of populations to evolve and adapt. The identification of evolutionarily significant units (ESUs) allows cryptic genetic diversity to be taken into account when designating conservation priorities. Here, we used mitochondrial and nuclear DNA sequences integrated with ecological niche models (ENM) to identify ESUs in Hypolestes trinitatis, a threatened Cuban endemic damselfly species. We found that this species comprises two distinct genetic groups in Central and Eastern Cuba respectively, which are also geographically isolated, as shown by ENM. Therefore, we propose these groups to be considered as different ESUs. According with their extent of occurrence, number of locations and inferred decline of habitat extent and quality, Central and Eastern ESUs qualify as Endangered [EN B1b(iii)] and Vulnerable [VU B1b(iii)], respectively.     

Introgressive hybridization erodes morphological divergence between lentic and lotic habitats in an endangered minnow

Introgressive hybridization may erode phenotypic divergence along environmental gradients, collapsing locally adapted populations into a hybrid swarm. Alternatively, introgression may promote phenotypic divergence by providing variation on which natural selection can act. In freshwater fishes, water flow often selects for divergent morphological traits in lake versus stream habitats. We tested the effects of introgression on lake–stream morphological divergence in the minnow Owens Tui Chub (Siphateles bicolor snyderi), which has been rendered endangered by introgession from the introduced Lahontan Tui Chub (Siphateles bicolor obesa). Using geometric morphometric analysis of 457 individual Tui Chub from thirteen populations, we found that both native and introgressing parent taxa exhibited divergent body and caudal fin shapes in lake versus stream habitats, but their trajectories of divergence were distinct. In contrast, introgressed populations exhibited intermediate body and caudal fin shapes that were not differentiated by habitat type, indicating that introgression has eroded phenotypic divergence along the lentic–lotic gradient throughout the historic range of the Owens Tui Chub. Individuals within hybrid populations were less morphologically variable than those within parent populations, suggesting hybrid adaptation to selective agents other than water flow or loss of variance by drift.     

Population divergence in plasticity of the AVT system and its association with aggressive behaviors in a Death Valley pupfish

Behavioral differences can evolve rapidly in allopatry, but little is known about the neural bases of such changes. Allopatric populations of Amargosa pupfish (Cyprinodon nevadensis) vary in aggression and courtship behaviors in the wild. Two of these wild populations were recently found to differ in brain expression of arginine vasotocin (AVT)--a peptide hormone shown previously to modulate aggression in pupfish. These populations have been isolated for less than 4000 years, so it remained unclear whether the differences in behavior and neural AVT phenotype were evolved changes or plastic responses to ecologically dissimilar habitats. Here, I tested whether these population differences have a genetic basis by examining how aggressive behavior and neural AVT phenotype responded to ecologically relevant variation in salinity (0.4 ppt or 3 ppt) and temperature (stable or daily fluctuating). Pupfish from Big Spring were more aggressive than pupfish from the Amargosa River when bred and reared under common laboratory conditions. Morphometric analysis of preoptic AVT immunoreactivity showed that the populations differed in how the AVT system responded to salinity and temperature conditions, and revealed that this plasticity differed between parvocellular and magnocellular AVT neuron groups. Both populations also showed relationships between neural AVT phenotype and aggression in the rearing environment, although populations differed in how aggression related to variation in magnocellular AVT neuron size. Together, these results demonstrate that the pupfish populations have diverged in how physical and social conditions affect the AVT system, and provide evidence that the AVT system can evolve quickly to ecologically dissimilar environments.