Craig A. Stockwell

Contemporary evolution meets conservation biology

Recent research has revealed that evolution often occurs on contemporary timescales, often within decades. Contemporary evolution is associated with the same factors that are driving the current extinction crisis: habitat loss and degradation, overharvesting and exotic species. Thus, it is relevant to many conservation situations. First, habitat fragmentation might influence the potential of a population to adapt in response environmental degradation. Second, certain harvesting strategies can result in the evolution of life-history traits, ultimately resulting in negative impacts on harvestable yield. Third, the establishment of exotic species can be influenced by their adaptive potential and our ability to limit that potential. Furthermore, contemporary evolution is of concern for intensively managed species, because it might reduce their fitness in native habitats. Ultimately, contemporary evolution is influenced by complex interactions among population size, genetic variation, the strength of selection, and gene flow, making most management scenarios unique. In a world filled with contemporary evolution, conservation efforts that ignore its implications will be less efficient and perhaps even risk prone. Humans have become an evolutionary force of extraordinary influence [1], evidenced most obviously by an unprecedented extinction rate that is attributable to their activities [2]. Human activities are also associated with evolutionary changes that can occur within a few hundred years, otherwise known as CONTEMPORARY EVOLUTION (see Glossary) [3‐5].

Contemporary evolution meets conservation biology II: impediments to integration and application

Conservation biology needs to be concerned not just with exogenous threats to populations, but also with the changing nature of populations themselves. In a previous review paper, we highlighted evolution in contemporary time (years to decades) as a largely overlooked aspect of population responses to environmental perturbations. We argued that these responses might affect the fate of natural, managed and exotic populations. In the present review, we discuss issues that may limit the integration of contemporary evolution into conservation biology—with the intent that recognition of these limitations may foster research, discussion and resolution. In particular, we consider (1) alternative perceptions of “evolutionary” and “ecological” time, (2) the role of contemporary evolution as an ecological process, (3) fitness as a bridge between evolution and conservation, and (4) challenges faced by conservation strategies based on gene flow estimation or manipulation. We close by highlighting some situations in which current conservation approaches and contemporary evolution may require reconciliation.

Morphological Divergence of Native and Recently Established Populations of White Sands Pupfish (Cyprinodon tularosa)

Abstract We used landmark-based geometric morphometric methods to describe patterns of body shape variation and shape covariation with size among populations of the threatened White Sands Pupfish (Cyprinodon tularosa), a species that occurs in dissimilar aquatic habitats. White Sands Pupfish populations include two genetically distinct, native populations that have been historically isolated in Salt Creek, a saline river, and Malpais Spring, a brackish spring. In addition, two populations were established approximately 30 years before this study by translocation of fish from Salt Creek to Lost River (a saline river) and Mound Spring (a brackish spring). We found significant body shape variation among populations and between males and females. Body shapes were more slender for females than for males and more slender for saline river populations than brackish spring populations. Introductions of pupfish to new habitats resulted in significant departures in body shape and shape allometry from the native Salt Creek population. Shape divergence was more pronounced for the Mound Spring population, which is consistent with a greater change in abiotic conditions. Although Mound Spring pupfish, like Malpais Spring pupfish, were more deep-bodied than saline river pupfish, differences in body shape and the level of sexual dimorphism were significant between the two brackish spring populations, indicating that deep-bodied shapes may be achieved from different anatomical configurations. The significant shape divergence of introduced populations warrants consideration for the conservation of this rare species, as creation of refuge populations for native stocks is a current management strategy.

Assessment of potential impacts of exotic species on populations of a threatened species, white sands pupfish, Cyprinodon tularosa.

The potential impact of introduced species on rare taxa is of particular concern to conservation biologists. We evaluate the impacts of western mosquitofish (Gambusia affinis) and virile crayfish (Orconectes virilis) on experimental populations of a threatened species, the White Sands pupfish (Cyprinodon tularosa). Forty experimental pupfish populations were exposed to one of four treatments; (a) 1 crayfish, (b) 4 crayfish, (c) 5 adult mosquitofish and (d) control. Pupfish population size and biomass was monitored over the duration of one breeding season. A repeated measure multiple analysis of covariance revealed a significant effect of treatments on response variables (population size and biomass) (P<0.0001). Mosquitofish had a significant effect on population size and biomass (P=0.0330). The effect of one crayfish was not significant (P=0. 0683). However, 4 crayfish had a significant effect (P<0.0001) on population size. We use these data, along with information on environmental tolerances of crayfish and mosquitofish, to evaluate risks for specific pupfish populations.

PHOSPHOGLUCONATE DEHYDROGENASE POLYMORPHISM AND SALINITY IN THE WHITE SANDS PUPFISH

The phosphogluconate dehydrogenase (Pgdh) locus is the only polymorphic allozyme locus observed among 37 loci examined in all four populations of a New Mexico state Endangered species, the White Sands pupfish (Cyprinodon tularosa). We report evidence suggesting that this polymorphism may be associated with salinity. Salinity levels vary widely within and between habitats occupied by White Sands pupfish. The frequency of the Pgdh100 allozyme was correlated with salinity but not with temperature. Frequency of Pgdh100 differed between low (3.76 parts per thousand (ppt)) and high (9.23 ppt) salinity sites at Malpais Spring despite no obvious barriers to fish movement. Frequencies of Pgdh100 in two introduced populations differed from that of the presumptive founding stock and correlated with salinity in the current habitats.

Evaluation of the introduction history and genetic diversity of a serially introduced fish population in New Zealand

Understanding the introduction history and the impact of founder events on invasive species is crucial to understanding the evolutionary mechanisms driving successful invasions. Recently, there has been increased discussion of the “paradox” of invasions, the high success of introduced populations that presumably have limited genetic diversity associated with founder events. The western mosquitofish Gambusia affinis is an ideal species for evaluating this paradox, because it has been widely introduced from its native range in central Texas, USA. This species was introduced to the North Island of New Zealand, circa 1930, and has since invaded aquatic habitats across the North Island. We conducted a microsatellite assay of populations from both the native and introduced range to verify the documented history of invasion and to assess the impact of serial introduction events on the genetic diversity of recently established New Zealand populations. The molecular data were consistent with the documented introduction history. In addition, we found sharp reductions in the allelic richness and the heterozygosity of the introduced populations relative to the original native populations, indicating the presence of founder effects. We also observed the development of strong genetic structure within the introduced range, which is absent within the native range. Finally, we applied approximate Bayesian computation to the introduction scenario to estimate the long-term effective population sizes for the sampled populations.

Parasites and salinity: costly tradeoffs in a threatened species

Parasites and environmental conditions can have direct and indirect effects on individuals. We explore the relationship between salinity and parasites in an endemic New Mexico State threatened fish, the White Sands pupfish (Cyprinodon tularosa). Spatial variation in salinity limits the distribution of the endemic springsnail (Juturnia tularosae) within Salt Creek, a small desert stream. The springsnail is the presumed intermediate host for trematodes that infect the White Sands pupfish, and trematode prevalence and intensity in pupfish are positively associated with the springsnail. Salinity and parasites both have negative impacts on pupfish, but in areas of high salinity, pupfish can effectively escape parasites. Pupfish trematodes were absent from sites lacking snails. At the upstream site, the absence of parasites and lower variance in salinity were correlated with larger pupfish that were in better condition than pupfish at either the middle or lower sites. Springsnails were present in the middle section, an area with moderate salinity, and all pupfish had trematodes (median abundance 847 trematodes/fish). Lipid levels and condition were lowest in fish from the middle site. Additionally, fewer older fish indicated an increased mortality rate. At the lower site, springsnails were absent due to high salinity; pupfish trematode abundance was much lower (six trematodes/fish), and fish condition was intermediate. An additional experiment revealed that snail activity and survival were significantly reduced at high salinities commonly present at the lower site. Although both high salinity and parasites significantly affect pupfish, parasites might be more detrimental.

Contemporary evolutionary divergence for a protected species following assisted colonization.

Background Contemporary evolution following assisted colonization may increase the probability of persistence for refuge populations established as a bet-hedge for protected species. Such refuge populations are considered “genetic replicates” that might be used for future re-colonization in the event of a catastrophe in the native site. Although maladaptive evolutionary divergence of captive populations is well recognized, evolutionary divergence of wild refuge populations may also occur on contemporary time scales. Thus, refuge populations may lose their “value” as true genetic replicates of the native population. Here, we show contemporary evolutionary divergence in body shape in an approximately 30-year old refuge population of the protected White Sands pupfish (Cyprinodon tularosa) resulting in a body-shape mismatch with its native environment. Methodology/Principal Findings Geometric morphometic data were collected from C. tularosa cultures raised in experimental mesocosms. Cultures were initiated with fish from the two native populations, plus hybrids, in high or low salinity treatments representing the salinities of the two native habitats. We found that body shape was heritable and that shape variation due to phenotypic plasticity was small compared to shape variation due to population source. C. tularosa from the high salinity population retained slender body shapes and fish from the low salinity population retained deep body shapes, irrespective of mesocosm salinity. These data suggest that the observed divergence of a recently established pupfish population was not explained by plasticity. An analysis of microsatellite variation indicated that no significant genetic drift occurred in the refuge population, further supporting the adaptive nature of changes in body shape. These lines of evidence suggest that body shape divergence of the refuge population reflects a case of contemporary evolution (over a 30-year period). Conclusions/Significance These results suggest assisted colonization can introduce novel, and/or relaxed selection, and lead to unintended evolutionary divergence.

Evaluating an icon of population persistence: the Devil's Hole pupfish

The Devils Hole pupfish Cyprinodon diabolis has iconic status among conservation biologists because it is one of the Worlds most vulnerable species. Furthermore, C. diabolis is the most widely cited example of a persistent, small, isolated vertebrate population; a chronic exception to the rule that small populations do not persist long in isolation. It is widely asserted that this species has persisted in small numbers (less than 400 adults) for 10 000–20 000 years, but this assertion has never been evaluated. Here, we analyse the time series of count data for this species, and we estimate time to coalescence from microsatellite data to evaluate this hypothesis. We conclude that mean time to extinction is approximately 360–2900 years (median 410–1800), with less than a 2.1% probability of persisting 10 000 years. Median times to coalescence varied from 217 to 2530 years, but all five approximations had wide credible intervals. Our analyses suggest that Devils Hole pupfish colonized this pool well after the Pleistocene Lakes receded, probably within the last few hundred to few thousand years; this could have occurred through human intervention.

An evaluation of the genetic structure and post-introduction dispersal of a non-native invasive fish to the North Island of New Zealand.

The efficacy of invasive species management is dependent on a thorough understanding of the size, origin, and genetic structure of invasive populations. We evaluated the genetic diversity and structure of the western mosquitofish, Gambusia affinis, across the North Island of New Zealand in an effort to better understand the genetic structure and post-introduction dispersal mechanisms of this highly invasive estuarine species. We found clear evidence of founder effects and significant genetic structure for populations derived from populations initially established in New Zealand in the 1930s. Our findings indicate that G. affinis populations have succeeded through a combination of localized dispersal and human-assisted colonization. Additionally, we identify a series of populations in one region that are apparently genetically isolated from the other regions. This area could thus represent a “significant eradication unit” where re-colonization is unlikely. Our results highlight the utility and value of molecular tools as an efficient method to facilitate a richer understanding of the nature and condition of invasive species while identifying definitive management objectives.