Simulating selection and evolution at the community level using common garden data.

A key issue in evolutionary biology is whether selection acting at levels higher than the individual can cause evolutionary change. If it can, then conceptual and empirical studies must consider how selection operates at multiple levels of biological organization. Here, we test the hypothesis that estimates of broad-sense community heritability, H C 2 , can be used to predict the evolutionary response by community-level phenotypes when community-level selection is imposed. Using an approach informed by classic quantitative genetics, we made three predictions. First, when we imposed community-level selection, we expected a significant change in the average phenotype of arthropod communities associated with individual tree genotypes [we imposed selection by favoring high and low NMDS (nonmetric multidimensional scaling) scores that reflected differences in arthropod species richness, abundance and composition]. Second, we expected H C 2 to predict the magnitude of the community-level response. Third, we expected no significant change in average NMDS scores with community-level selection imposed at random. We tested these hypotheses using three years of common garden data for 102 species comprising the arthropod communities, associated with nine clonally replicated Populus angustifolia genotypes. Each of our predictions were met. We conclude that estimates of H C 2 account for the resemblance among communities sharing common ancestry, the persistence of community composition over time, and the outcome of selection when it occurs at the community level. Our results provide a means for exploring how this process leads to large-scale community evolutionary change, and they identify the circumstances in which selection may routinely act at the community level.

Local adaptation and rapid evolution of aphids in response to genetic interactions with their cottonwood hosts.

Several studies have demonstrated the ecological consequences of genetic variation within a single plant species. For example, these studies show that individual plant genotypes support unique composition of the plants' associated arthropod community. By contrast, fewer studies have explored how plant genetic variation may influence evolutionary dynamics in the plant's associated species. Here, we examine how aphids respond evolutionarily to genetic variation in their host plant. We conducted two experiments to examine local adaptation and rapid evolution of the free-feeding aphid Chaitophorus populicola across genetic variants of its host plant, Populus angustifolia. To test for local adaptation, we collected tree cuttings and aphid colonies from three sites along an elevation/climate gradient and conducted a reciprocal transplant experiment. In general, home aphids (aphids transplanted onto trees from the same site) produced 1.7-3.4 times as many offspring as foreign aphids (aphids transplanted onto trees from different sites). To test for rapid evolution, we used 4 clonally replicated aphid genotypes and transplanted each onto 5 clonally replicated P. angustifolia genotypes. Each tree genotype started with the same aphid genotype composition. After 21 days (~two aphid generations), aphid genotype composition changed (i.e., aphids evolved) and some tree genotypes supported unique evolutionary trajectories of aphids. These results suggest that plant evolution in response to human perturbation, such as climate change and invasive species, will also result in evolutionary responses in strongly interacting species that could cascade to affect whole communities.

Dialects in the alarm calls of black- tailed prairie dogs (Cynomys ludovicianus): A case of cultural diffusion?

Prairie dogs (Cynomys spp.) produce an alarm call when a predator appears. Gunnison's prairie dogs (Cynomys gunnisoni) produce calls that vary in spectral structure according to predator type and specific characteristics unique to the individual predator, such as color and shape. These calls vary depending on geographic location and have been characterized as dialects. Black-tailed prairie dogs (Cynomys ludovicianus) also encode information about terrestrial predators in their alarm calls. However, nothing is known about whether there are dialects in these alarm calls, and if so, why these dialects might have arisen. We studied the alarm calls and habitat characteristics of eight different black-tailed prairie dog colonies within the Southwestern USA: Maxwell National Wildlife Refuge, NM, Vermejo Park Ranch, NM, Kiowa National Grasslands, NM, Rita Blanca National Grasslands, TX, and Comanche National Grasslands, CO. An analysis of time and frequency changes in alarm calls showed that colony sites that were located within 30 km each other did not have significant differences in alarm call structure, but sites that were more distant were significantly different from the other sites, consistent with the existence of dialects as well as with genetic models of isolation by distance. The acoustic structure of the alarm calls was not explained by differences in habitat characteristics at each site. A comparison of Squared Euclidian Distances (D2) of alarm calls versus linear distances between sites showed a significant positive correlation, implying that alarm call dialect differences increase the farther one site is from another. This relationship is consistent with a cultural diffusion model of dialects, and is similar to that observed in human dialects.

Population survey and management strategies of free-roaming dogs (Canis familiaris) on Saipan, Commonwealth of the Northern Mariana Islands.

The island of Saipan, Commonwealth of the Northern Mariana Islands, is populated by free-roaming dogs who were introduced during World War II. The local nonhuman animal control agency manages this population; however, the demographic information and public perception of this population remain unknown. To characterize the free-roaming dog population, an island-wide survey on Saipan was conducted. Photographic, mark-recapture data were used to estimate the population size per land type. Age, sex, sociality, and behavior per land type were documented and associations between these variables were tested using G tests. The effects of land type and urbanization on dog abundance were also analyzed. Lastly, in-person surveys provided data on the public perception of free-roaming dogs. Four main findings are reported: (a) The population size of free-roaming dogs on Saipan is estimated at 21,316. (b) Most dogs encountered were sentry adults. (c) Dog abundance increased with urbanization level and was highest in urban areas. (d) The public perceived free-roaming dogs as a health concern and suggested the implementation of leash laws and sheltering initiatives. This article discusses potential and existing population management strategies for free-roaming dogs on Saipan.

The opportunity for sexual selection and the evolution of non-responsiveness to pesticides, sterility inducers and contraceptives.

We illustrate a method for delaying and possibly eliminating the evolution of non-responsiveness to the treatments now used to control pest populations. Using simulations and estimates of the variance in relative fitness, i.e., the opportunity for selection, in a rat-like mammal, we show that the selection responsible for the evolution of non-responsiveness to pesticides and sterility-inducers, is similar in its action to sexual selection, and for this reason can be orders of magnitude stronger than that which exists for untreated populations. In contrast, we show that when contraceptives are used to reduce the fertility of a pest species, with non-responders embedded within such populations, the opportunity for selection favoring non-responsiveness is reduced to that which is expected by chance alone. In pest species with separate sexes, we show that efforts to control pest populations or to mitigate selection favoring non-responsiveness, are likely to be ineffective when members of one sex are sterilized or killed. We also show that while mating preferences can impede the rate at which resistance evolves, they are more likely to accelerate this process, arguing against the use of sterile male approaches for controlling pests. Our results suggest that contraceptives are more effective at controlling pest populations and slowing the evolution of non-responsiveness than treatments that cause sterilization or death in target species. Furthermore, our results indicate that contraceptives that work differentially on each sex will be most effective in mitigating selection favoring non-responders. Our results have significant implications for the development and application of treatments to manage pests, now and into the future.

Helobdella blinni sp. n. (Hirudinida, Glossiphoniidae) a new species inhabiting Montezuma Well, Arizona, USA.

A new leech species Helobdella blinnisp. n., is described from Montezuma Well, an isolated travertine spring mound located in central Arizona, USA. In its native habitat, Helobdella blinni had been previously identified as Helobdella stagnalis (Linnaeus, 1758), which was later reclassified to Helobdella modesta (Verrill, 1872). Similar to the European Helobdella stagnalis and North American Helobdella modesta, Helobdella blinni has six pairs of testisacs, five pairs of smooth crop caecae, one lobed pair of posteriorly-directed crop caecae, one pair of eyes, a nuchal scute, and diffuse salivary glands. However, the pigmentation of this new species ranges from light to dark brown, unlike Helobdella modesta which tends to be light grey in color. Also, Helobdella modesta produces a clutch of 12--35 pink eggs, whereas Helobdella blinni produces smaller clutches of white eggs (7-14, 0.5 ± 0.15 mm, N = 7) and consequently broods fewer young (1-14, 7 ± 3.3 mm, N = 97). Helobdella blinni are also able to breed year-round due to the constant warm water conditions in Montezuma Well. Their breeding season is not restricted by seasonal temperatures. These species are morphologically similar, however, comparing the COI mtDNA sequences of Helobdella blinni with sequences from nearby populations of Helobdella modesta and other Helobdella species from GenBank indicate that Helobdella blinni is genetically distinct from these other Helobdella populations.

Genetically informed ecological niche models improve climate change predictions.

We examined the hypothesis that ecological niche models (ENMs) more accurately predict species distributions when they incorporate information on population genetic structure, and concomitantly, local adaptation. Local adaptation is common in species that span a range of environmental gradients (e.g., soils and climate). Moreover, common garden studies have demonstrated a covariance between neutral markers and functional traits associated with a species' ability to adapt to environmental change. We therefore predicted that genetically distinct populations would respond differently to climate change, resulting in predicted distributions with little overlap. To test whether genetic information improves our ability to predict a species' niche space, we created genetically informed ecological niche models (gENMs) using Populus fremontii (Salicaceae), a widespread tree species in which prior common garden experiments demonstrate strong evidence for local adaptation. Four major findings emerged: (i) gENMs predicted population occurrences with up to 12-fold greater accuracy than models without genetic information; (ii) tests of niche similarity revealed that three ecotypes, identified on the basis of neutral genetic markers and locally adapted populations, are associated with differences in climate; (iii) our forecasts indicate that ongoing climate change will likely shift these ecotypes further apart in geographic space, resulting in greater niche divergence; (iv) ecotypes that currently exhibit the largest geographic distribution and niche breadth appear to be buffered the most from climate change. As diverse agents of selection shape genetic variability and structure within species, we argue that gENMs will lead to more accurate predictions of species distributions under climate change.

Genotypic variation in foundation species generates network structure that may drive community dynamics and evolution.

Although genetics in a single species is known to impact whole communities, little is known about how genetic variation influences species interaction networks in complex ecosystems. Here, we examine the interactions in a community of arthropod species on replicated genotypes (clones) of a foundation tree species, Populus angustifolia James (narrowleaf cottonwood), in a long-term, common garden experiment using a bipartite "genotype-species" network perspective. We combine this empirical work with a simulation experiment designed to further investigate how variation among individual tree genotypes can impact network structure. Three findings emerged: (1) the empirical "genotype-species network" exhibited significant network structure with modularity being greater than the highly conservative null model; (2) as would be expected given a modular network structure, the empirical network displayed significant positive arthropod co-occurrence patterns; and (3) furthermore, the simulations of "genotype-species" networks displayed variation in network structure, with modularity in particular clearly increasing, as genotypic variation increased. These results support the conclusion that genetic variation in a single species contributes to the structure of ecological interaction networks, which could influence eco-ogical dynamics (e.g., assembly and stability) and evolution in a community context.

Climate change perils for dioecious plant species.

Climate change, particularly increased aridity, poses a significant threat to plants and the biotic communities they support. Dioecious species may be especially vulnerable to climate change given that they often exhibit spatial segregation of the sexes, reinforced by physiological and morphological specialization of each sex to different microhabitats. In dimorphic species, the overexpression of a trait by one gender versus the other may become suppressed in future climates. Data suggest that males will generally be less sensitive to increased aridity than co-occurring females and, consequently, extreme male-biased sex ratios are possible in a significant number of populations. The effects of male-biased sex ratios are likely to cascade to dependent community members, especially those that are specialized on one sex.

The Opportunity for Post-Copulatory Sexual Selection in the Ectoparasitic Pea Crab, Dissodactylus primitivus (Brachyura: Pinnotheridae).

Pea crabs, Dissodactylus primitivus, inhabit multiple echinoid (heart urchin) hosts. Male and female crabs move among hosts in search for mates, and both sexes mate multiple times, creating opportunities for post-copulatory sexual selection. For such selection to occur, only a fraction of the males who succeed in mating can also succeed in siring progeny. Jossart et al. 2014 used 4 microsatellite loci to document parentage and mating frequencies of both sexes in D. primitivus. From these data we identified the mean and variance in female offspring numbers, as well as the proportions of the female population that were gravid and not bearing offspring. We next identified the proportions of the male population who had (1) mated and sired offspring, (2) mated but failed to sire offspring, and (3) failed to mate altogether. We used these results to estimate the opportunity for selection on males and females in terms of mate numbers and offspring numbers, and estimated the sex difference in the opportunity for selection (i.e., the opportunity for sexual selection) using both forms of data. We then partitioned the total variance in male fitness into pre- and post-copulatory components and identified the fraction of the total opportunity for selection occurring in each context. Our results show that the opportunity for selection on each sex was of similar magnitude (0.69-0.98), consistent with this polyandrogynous mating system. We also found that 37% of the total opportunity for sexual selection on males occurred within the context of post-copulatory sexual selection. However, the fraction of the total opportunity for selection that was due to sexual selection, estimated using both mate numbers and offspring numbers, was 9% and 23% respectively. Thus, we further reduced our estimate of the opportunity for post-copulatory sexual selection in D. primitivus to less than 10% of the total opportunity for selection (0.37 of 0.09 and 0.23 = 0.03 and 0.09). Our results provide the first estimate of the maximum possible strength of post-copulatory sexual selection in crustaceans using this approach.

Rapid plant evolution in the presence of an introduced species alters community composition.

Because introduced species may strongly interact with native species and thus affect their fitness, it is important to examine how these interactions can cascade to have ecological and evolutionary consequences for whole communities. Here, we examine the interactions among introduced Rocky Mountain elk, Cervus canadensis nelsoni, a common native plant, Solidago velutina, and the diverse plant-associated community of arthropods. While introduced species are recognized as one of the biggest threats to native ecosystems, relatively few studies have investigated an evolutionary mechanism by which introduced species alter native communities. Here, we use a common garden design that addresses and supports two hypotheses. First, native S. velutina has rapidly evolved in the presence of introduced elk. We found that plants originating from sites with introduced elk flowered nearly 3 weeks before plants originating from sites without elk. Second, evolution of S. velutina results in a change to the plant-associated arthropod community. We found that plants originating from sites with introduced elk supported an arthropod community that had ~35 % fewer total individuals and a different species composition. Our results show that the impacts of introduced species can have both ecological and evolutionary consequences for strongly interacting species that subsequently cascade to affect a much larger community. Such evolutionary consequences are likely to be long-term and difficult to remediate.

Incorporating climate change and exotic species into forecasts of riparian forest distribution.

We examined the impact climate change (CC) will have on the availability of climatically suitable habitat for three native and one exotic riparian species. Due to its increasing prevalence in arid regions throughout the western US, we predicted that an exotic species, Tamarix, would have the greatest increase in suitable habitat relative to native counterparts under CC. We used an ecological niche model to predict range shifts of Populus fremontii, Salix gooddingii, Salix exigua and Tamarix, from present day to 2080s, under five general circulation models and one climate change scenario (A1B). Four major findings emerged. 1) Contrary to our original hypothesis, P. fremontii is projected to have the greatest increase in suitable habitat under CC, followed closely by Tamarix. 2) Of the native species, S. gooddingii and S. exigua showed the greatest loss in predicted suitable habitat due to CC. 3) Nearly 80 percent of future P. fremontii and Salix habitat is predicted to be affected by either CC or Tamarix by the 2080s. 4) By the 2080s, 20 percent of S. gooddingii habitat is projected to be affected by both Tamarix and CC concurrently, followed by S. exigua (19 percent) and P. fremontii (13 percent). In summary, while climate change alone will negatively impact both native willow species, Tamarix is likely to affect a larger portion of all three native species' distributions. We discuss these and other results in the context of prioritizing restoration and conservation efforts to optimize future productivity and biodiversity. As we are accounting for only direct effects of CC and Tamarix on native habitat, we present a possible hierarchy of effects- from the direct to the indirect- and discuss the potential for the indirect to outweigh the direct effects. Our results highlight the need to account for simultaneous challenges in the face of CC.

How multiple mating by females affects sexual selection.

Multiple mating by females is widely thought to encourage post-mating sexual selection and enhance female fitness. We show that whether polyandrous mating has these effects depends on two conditions. Condition 1 is the pattern of sperm utilization by females; specifically, whether, among females, male mating number, m (i.e. the number of times a male mates with one or more females) covaries with male offspring number, o. Polyandrous mating enhances sexual selection only when males who are successful at multiple mating also sire most or all of each of their mates' offspring, i.e. only when Cov(♂)(m,o), is positive. Condition 2 is the pattern of female reproductive life-history; specifically, whether female mating number, m, covaries with female offspring number, o. Only semelparity does not erode sexual selection, whereas iteroparity (i.e. when Cov(♀)(m,o), is positive) always increases the variance in offspring numbers among females, which always decreases the intensity of sexual selection on males. To document the covariance between mating number and offspring number for each sex, it is necessary to assign progeny to all parents, as well as identify mating and non-mating individuals. To document significant fitness gains by females through iteroparity, it is necessary to determine the relative magnitudes of male as well as female contributions to the total variance in relative fitness. We show how such data can be collected, how often they are collected, and we explain the circumstances in which selection favouring multiple mating by females can be strong or weak.

Differences in relative fitness among alternative mating tactics might be more apparent than real.

Two theoretical frameworks guide research on multiple male phenotypes within natural populations. Each scheme recognizes that male polymorphisms vary in the degree to which genotype and environment influence trait expression. Consensus remains elusive, however, on whether average fitnesses must be equivalent and whether genetic differences need exist for polymorphism to persist over time. Schradin and Lindholm address these hypotheses in African four-striped mice with detailed parentage and body size data. Their results and interpretation call each framework's predictions into question, but reveal a common truth. Debate might be resolved if researchers agreed on which parameters to measure and compare.

Sexual selection and mating systems.

Sexual selection is among the most powerful of all evolutionary forces. It occurs when individuals within one sex secure mates and produce offspring at the expense of other individuals within the same sex. Darwin was first to recognize the power of sexual selection to change male and female phenotypes, and, in noting that sexual selection is nonubiquitous, Darwin was also first to recognize the importance of mating system--the "special circumstances" in which reproduction occurs within species. Analyses of mating systems since Darwin have emphasized either the genetic relationships between male and female mating elements, usually among plants, or the numbers of mates males and females may obtain, usually among animals. Combining these schemes yields a quantitative methodology that emphasizes measurement of the sex difference in the variance in relative fitness, as well as phenotypic and genetic correlations underlying reproductive traits that may arise among breeding pairs. Such information predicts the degree and direction of sexual dimorphism within species, it allows the classification of mating systems using existing genetic and life history data, and with information on the spatial and temporal distributions of fertilizations, it may also predict floral morphology in plants. Because this empirical framework identifies selective forces and genetic architectures responsible for observed male-female differences, it compliments discoveries of nucleotide sequence variation and the expression of quantitative traits. Moreover, because this methodology emphasizes the process of evolutionary change, it is easier to test and interpret than frameworks emphasizing parental investment in offspring and its presumed evolutionary outcomes.

Tree hybridization and genotypic variation drive cryptic speciation of a specialist mite herbivore.

Few studies have investigated the roles that plant hybridization and individual plant genotype play in promoting population divergence within arthropod species. Using nrDNA sequence information and reciprocal transfer experiments, we examined how tree cross type (i.e., pure Populus angustifolia and P. angustifolia x P. fremontii F(1) type hybrids) and individual tree genotype influence host race formation in the bud-galling mite Aceria parapopuli. Three main findings emerged: (1) Strong genetic differentiation of mite populations found on pure P. angustifolia and F(1) type hybrids indicates that these mites represent morphologically cryptic species. (2) Within the F(1) type hybrids, population genetic analyses indicate migration among individual trees; however, (3) transfer experiments show that the mites found on heavily infested F(1) type trees perform best on their natal host genotype, suggesting that genetic interactions between mites and their host trees drive population structure, local adaptation, and host race formation. These findings argue that hybridization and genotypic differences in foundation tree species may drive herbivore population structure, and have evolutionary consequences for dependent arthropod species.

Extending genomics to natural communities and ecosystems.

An important step in the integration of ecology and genomics is the progression from molecular studies of relatively simple model systems to complex field systems. The recent availability of sequenced genomes from key plants is leading to a new understanding of the molecular drivers of community composition and ecosystem processes. As genome sequences accumulate for species that form intimate associations in nature, a detailed view may emerge as to how these associations cause changes among species at the nucleotide level. This advance could dramatically alter views about the structure and evolution of communities and ecosystems.

A framework for community and ecosystem genetics: from genes to ecosystems.

Can heritable traits in a single species affect an entire ecosystem? Recent studies show that such traits in a common tree have predictable effects on community structure and ecosystem processes. Because these 'community and ecosystem phenotypes' have a genetic basis and are heritable, we can begin to apply the principles of population and quantitative genetics to place the study of complex communities and ecosystems within an evolutionary framework. This framework could allow us to understand, for the first time, the genetic basis of ecosystem processes, and the effect of such phenomena as climate change and introduced transgenic organisms on entire communities.

Don'T throw bateman out with the bathwater!

Bateman identified two aspects of sexual selection. The first, called Bateman's principle, is that sexual selection favors increased promiscuity of males but not of females as a result of differences in parental investment in gametes. The second is that the variance in mate number of males is the fundamental cause of a sex difference in fitness variance. We argue that Bateman's insight about the source of sexual selection is more fundamental than his speculation about patterns of parental investment. We show that, when the sex ratio is 1:1, the average female must be as promiscuous as the average male, because each copulation involves one male and one female. Because mean male and female promiscuity are tied together in the same manner as mean male and female fitness, a sex difference in mating propensity must be the result of either (1) a sex difference in the covariance between matings and number offspring, or (2) Fisherian run-away sexual selection, wherein female reluctance to mate is a weak form of female choice. We show how female promiscuity can limit the evolution of male promiscuity, turning the central argument of parental investment theory on its head.

Fractal geometry is heritable in trees.

Understanding the genetic basis to landscape vegetation structure is an important step that will allow us to examine ecological and evolutionary processes at multiple spatial scales. Here for the first time we show that the fractal architecture of a dominant plant on the landscape exhibits high broad-sense heritability and thus has a genetic basis. The fractal architecture of trees is known to influence ecological communities associated with them. In a unidirectional cottonwood-hybridizing complex (Populus angustifolia x P. fremontii) pure and hybrid cottonwoods differed significantly in their fractal architecture, with phenotypic variance among backcross hybrids exceeding that of F1 hybrids and of pure narrowleaf cottonwoods by two-fold. This result provides a crucial link between genes and fractal scaling theory, and places the study of landscape ecology within an evolutionary framework.