Beyond Pairwise Interactions: Multispecies Character Displacement in Mexican Freshwater Fish Communities.

Competition has long been recognized as a central force in shaping evolution, particularly through character displacement. Yet research on character displacement is biased, as it has focused almost exclusively on pairs of interacting species while ignoring multispecies interactions. Communities are seldom so simple that only pairs of species interact, and it is not clear whether inferences from pairwise interactions are sufficient to explain patterns of phenotypes in nature. Here, we test for character displacement in a natural system of freshwater fishes in western Mexico that contains up to four congeneric species of the genus Poeciliopsis. We analyzed body shape differences between populations with different numbers of competitors while accounting for confounding environmental variables. Surprisingly, we found evidence for convergent character displacement in populations of P. prolifica, P. viriosa, and P. latidens. We also found that the convergence in body shape was not consistently in the same direction, meaning that when three or more competitors co-occurred, we did not find more extreme body shapes compared with when there were only two competitors. Instead, when three or more competitors co-occurred, body shape was intermediate between the shape found with a pair of species and the shape found with no competitor present. This intermediate shape suggests that evolution in multispecies communities likely occurs in response to several competitors rather than to simple pairwise interactions. Overall, our results suggest that competition among multiple species is more complex than simple pairwise competitive interactions.

Isotopic discrimination between carrion and elytra clippings of lab-reared American burying beetles (Nicrophorus americanus): Implications for conservation and evaluation of feeding relationships in the wild.

RATIONALE: Differences in stable isotope composition between an animal and its diet are quantified by experimentally derived diet-tissue discrimination factors. Appropriate discrimination factors between consumers and prey are essential for interpreting stable isotope patterns in ecological studies. While available for many taxa, these values are rarely estimated for organisms within the carrion food web. METHODS: We used a controlled-diet stable isotope feeding trial to quantify isotopic diet-tissue discrimination factors of carbon (δ13 C values) and nitrogen (δ15 N values) from laboratory-reared Nicrophorus americanus raised on carrion. We used exoskeleton samples of beetle elytra (wing covers) to determine diet-tissue discrimination factors using a continuous flow isotope ratio mass spectrometer equipped with an elemental analyzer. We also measured the isotopic compositions of five species of co-occurring, wild-caught burying beetles and evaluated feeding relationships. RESULTS: We found differences in stable carbon discrimination between carrion sources (mammalian and avian) and lab-reared beetles, but no difference in stable nitrogen discrimination. Values for δ13 C did not differ among wild-caught burying beetle species, but values for δ15 N were significantly different for the three species with overlapping breeding seasons. Furthermore, wild-caught burying beetles within our study area do not appear to use avian carrion resources to rear their young. CONCLUSIONS: This study informs future interpretation of stable isotope data for insects within the carrion food web. In addition, these results provide insight into carrion resources used by co-occurring burying beetle species in situ. We also demonstrated that independent of adult food type, the larval food source has a significant impact on the isotopic signatures of adult beetles, which can be estimated using a minimally invasive elytra clipping.

Multivariate heritability of shape in June sucker (Chasmistes liorus) and Utah sucker (Catostomus ardens): shape as a functional trait for discriminating closely related species.

Molecular genetic data suggest that June sucker (Chasmistes liorus) is only shallowly diverged from the co-occurring but phenotypically distinct Utah sucker (Catostomus ardens) in Utah Lake. Phenotypes representing both extreme morphologies (June sucker and Utah sucker) are observed in the small wild population, but relatively large numbers of intermediate phenotypes are also present. This relatively continuous variation between the two putative species could result from extensive hybridization (including reticulate evolutionary patterns) of genetically based phenotypes or incomplete divergence among lineages and extensive phenotypic plasticity with little genetic basis. To help inform the evolutionary history of June sucker and to provide critical information for management and restoration of June sucker populations, we evaluated the distribution of shape phenotypes among purebreds of each species and their hybrids and determined the heritability of shape and ecological performance between June sucker (C. liorus) and its sister species Utah sucker (C. ardens). Mouth shape of purebred June sucker and Utah sucker are located at the extremes, and hybrids are located midway between the purebreds. Multivariate heritability was relatively high for mouth shape at 0.27. Heritability for growth rate was high at 0.32-0.42, but variation was not associated with cross type. Genetically based variation in mouth shape has evolved fairly rapidly or has been maintained in the face of ongoing hybridization between the two species. Currently, there seems to be little evidence for differential selection between species that would maintain shape variation.

Heterochronic shift in gene expression leads to ontogenetic morphological divergence between two closely related polyploid species.

Heterochrony-alteration to the rate or timing of development-is an important mechanism of trait differentiation associated with speciation. Heterochrony may explain the morphological divergence between two polyploid species, June sucker (Chasmistes liorus) and Utah sucker (Catostomus ardens). The larvae of both species have terminal mouths; however, as adults, June sucker and Utah sucker develop subterminal and ventral mouths, respectively. We document a difference in the timing of shape development and a corresponding change in the timing of gene expression, suggesting the distinctive mouth morphology in June suckers may result from paedomorphosis. Specifically, adult June suckers exhibit an intermediate mouth morphology between the larval (terminal) and ancestral (ventral) states. Endemic and sympatric Chasmistes/Catostomus pairs in two other lakes also are morphologically divergent, but genetically similar. These species pairs could have resulted from the differential expression of genes and corresponding divergence in trait development. Paedomorphosis may lead to adaptive diversification in Catostomids.

Revisiting the ecology and evolution of burying beetle behavior (Staphylinidae: Silphinae).

Investigating fundamental processes in biology requires the ability to ground broad questions in species-specific natural history. This is particularly true in the study of behavior because an organism's experience of the environment will influence the expression of behavior and the opportunity for selection. Here, we provide a review of the natural history and behavior of burying beetles of the genus Nicrophorus to provide the groundwork for comparative work that showcases their remarkable behavioral and ecological diversity. Burying beetles have long fascinated scientists because of their well-developed parenting behavior, exhibiting extended post-hatching care of offspring that varies extensively within and across taxa. Despite the burgeoning success of burying beetles as a model system for the study of behavioral evolution, there has not been a review of their behavior, ecology, and evolution in over 25 years. To address this gap, we leverage a developing community of researchers who have contributed to a detailed knowledge of burying beetles to highlight the utility of Nicrophorus for investigating the causes and consequences of social and behavioral evolution.

Predation affects body shape in the knife livebearer Alfaro cultratus (Cyprinodontiformes: Poeciliidae).

Livebearing fishes are a common model for studying the effects of predation on prey biology. Numerous studies have found differences in life history, sexual selection, behavior, and morphology between populations of the same species that co-occur with predators and those that do not. Alfaro cultratus is a livebearing fish with populations in different predation environments, but unlike other livebearers, this species also has an extreme body shape that is laterally compressed. Given this unusual morphology, we asked if predation environment would still predict overall body shape, as has been documented in other species. We collected specimens from both predator and no predator sites in Costa Rica and used a geometric morphometrics analysis to determine if body shape is affected by predation environment, while controlling for size and river gradient. Body shape does indeed differ between predation environments; however, the observed differences contrast with the patterns found in other livebearer systems. Alfaro cultratus in predation environments had deeper and shorter bodies and deeper caudal peduncles than those found in environments without dominant fish predators.

Phylogenetic relationships of three rockfish: Sebastesmelanops, Sebastesciliatus and Sebastesvariabilis (Scorpaeniformes, Scorpaenidae) based on complete mitochondrial genome sequences.

We characterise the complete mitochondrial genomes (mitogenomes) of Black rockfish (Sebastesmelanops Girard, 1856; n = 1), Dark rockfish (Sebastesciliatus Tilesius, 1813; n = 2) and Dusky rockfish (Sebastesvariabilis Pallas, 1814; n = 2). The lengths of the mitogenomes are 16,405 bp for S.melanops, 16,400 bp for both S.ciliatus and 16,400 and 16,401 bp for S.variabilis. We examine these species' phylogenetic relationships using 35 previously published rockfish mitogenomes, representing 27 species. We find that S.melanops is sister to a clade consisting of S.rubrivinctus, S.nigrocinctus, S.umbrosus and S.oculatus, whereas S.ciliatus and S.variabilis are sister to a clade consisting of S.norvegicus, S.viviparus, S.mentella and S.fasciatus. We were unable to separate S.ciliatus and S.variabilis using their complete mitogenomes.

Multiple predators indirectly alter community assembly across ecological boundaries.

Models of habitat selection often assume that organisms choose habitats based on their intrinsic quality, regardless of the position of these habitats relative to low-quality habitats in the landscape. We created a habitat matrix in which high-quality (predator-free) aquatic habitat patches were positioned adjacent to (predator-associated) or isolated from (control) patches with single or two species of caged predators. After 16 days of colonization, larval insect abundance was reduced by 50% on average in both the predator and predator-associated treatments relative to isolated controls. Effects were largely similar among predator treatments despite variation in number of predator species, predator biomass, and whether predators were native or nonnative. Importantly, the strength of effects did not depend on whether predators were physically present. These results demonstrate that predator cues can cascade with equal strength across ecological boundaries, indirectly altering community assembly via habitat selection in intrinsically high-quality habitats.

Complete mitochondrial genomes of two rockfish: Sebastes maliger and Sebastes norvegicus (Scorpaenidae, Scorpaeniformes).

We report the complete mitochondrial genomes of two rockfish: Sebastes maliger and Sebastes norvegicus. The mitogenomes consist of 13 protein-coding regions, 22 tRNAs, two rRNAs, and one control region. Sebastes mitogenome control regions are highly variable due to the presence of repeat sequences. The mitogenomes for S. maliger and S. norvegicus are 16,403 and 16,401 bp, respectively. Using these two mitogenomes and 25 additional Sebastes mitogenomes from GenBank, we examine the phylogenetic relationships in Sebastes. Sebastes maliger is sister to a clade including S. rubrivinctus, S. nigrocinctus, S. umbrosus, and S. oculatus, while S. norvegicus is sister to S. fasciatus.

Complete mitochondrial genomes of June sucker and Utah sucker (Chasmistes liorus and Catostomus ardens).

The relationship between June sucker (Chasmistes liorus, Jordan, 1878) and Utah sucker (Catostomus ardens, Jordan & Gilbert, 1881) has been a matter of controversy since the mid 1900s. Chasmistes liorus is endemic to Utah Lake, UT and has a subterminal mouth adapted for pelagic feeding. Catostomus ardens is widely distributed throughout the Bonneville Basin and Upper Snake River Basin and has a ventral mouth adapted for benthic feeding. Chasmistes has been recognized as a separate ancient genus. Despite being morphologically distinct, no study has successfully identified residual genetic markers that separate these species. Of these studies, several have used a subset of mitochondrial genes, but no study has analyzed the complete mitochondrial genomes (mitogenomes) of these suckers (Pisces: Catostomidae). To further explore the genetic relationships between these species, we report the complete mitogenomes of Chasmistes liorus and Catostomus ardens. DNA was sequenced using an Illumina HiSeq 2500 system and mitogenomes were assembled and annotated using Geneious v. 2021.2 and MitoAnnotator, respectively. The mitogenomes of Chasmistes liorus and Catostomus ardens are both 16,623 bp and are ∼0.072% divergent. We examine the phylogenetic relationship between Chasmistes liorus and Catostomus ardens using 33 mitogenomes, representing 16 species, from Catostomidae. Our data suggest that Chasmistes liorus is sister to Catostomus ardens. Additional samples from multiple localities and/or cohorts of these species will allow us to better resolve the complicated phylogenetic relationships between these species.

No evidence for increased fitness of offspring from multigenerational effects of parental size or natal carcass size in the burying beetle Nicrophorus marginatus.

Multigenerational effects (often called maternal effects) are components of the offspring phenotype that result from the parental phenotype and the parental environment as opposed to heritable genetic effects. Multigenerational effects are widespread in nature and are often studied because of their potentially important effects on offspring traits. Although multigenerational effects are commonly observed, few studies have addressed whether they affect offspring fitness. In this study we assess the effect of potential multigenerational effects of parental body size and natal carcass size on lifetime fitness in the burying beetle, Nicrophorus marginatus (Coleoptera; Silphidae). Lifespan, total number of offspring, and number of offspring in the first reproductive bout were not significantly related to parental body size or natal carcass size. However, current carcass size used for reproduction was a significant predictor for lifetime number of offspring and number of offspring in the first brood. We find no evidence that multigenerational effects from larger parents or larger natal carcasses contribute to increased fitness of offspring.

Ontogenetic shape trajectory of Trichomycterus areolatus varies in response to water velocity environment.

Body and head shape among fishes both vary between environments influenced by water velocity and across ontogeny. Although the shape changes associated with variation in average water velocity and ontogeny are well documented, few studies have tested for the interaction between these two variables (i.e., does ontogenetic shape variation differ between velocity environments). We use geometric morphometrics to characterize shape differences in Trichomycterus areolatus, a freshwater catfish found in high and low-velocity environments in Chile. We identify a significant interaction between velocity environment and body size (i.e., ontogeny). Ontogenetic patterns of shape change are consistent with other studies, but velocity environment differentially affects the ontogenetic trajectory of shape development in T. areolatus. Shape change over ontogeny appears more constrained in high-velocity environments compared to low-velocity environments.

Behavioral constraints on local adaptation and counter-gradient variation: Implications for climate change.

Resource allocation to growth, reproduction, and body maintenance varies within species along latitudinal gradients. Two hypotheses explaining this variation are local adaptation and counter-gradient variation. The local adaptation hypothesis proposes that populations are adapted to local environmental conditions and are therefore less adapted to environmental conditions at other locations. The counter-gradient variation hypothesis proposes that one population out performs others across an environmental gradient because its source location has greater selective pressure than other locations. Our study had two goals. First, we tested the local adaptation and counter-gradient variation hypotheses by measuring effects of environmental temperature on phenotypic expression of reproductive traits in the burying beetle, Nicrophorus orbicollis Say, from three populations along a latitudinal gradient in a common garden experimental design. Second, we compared patterns of variation to evaluate whether traits covary or whether local adaptation of traits precludes adaptive responses by others. Across a latitudinal range, N. orbicollis exhibits variation in initiating reproduction and brood sizes. Consistent with local adaptation: (a) beetles were less likely to initiate breeding at extreme temperatures, especially when that temperature represents their source range; (b) once beetles initiate reproduction, source populations produce relatively larger broods at temperatures consistent with their local environment. Consistent with counter-gradient variation, lower latitude populations were more successful at producing offspring at lower temperatures. We found no evidence for adaptive variation in other adult or offspring performance traits. This suite of traits does not appear to coevolve along the latitudinal gradient. Rather, response to selection to breed within a narrow temperature range may preclude selection on other traits. Our study highlights that N. orbicollis uses temperature as an environmental cue to determine whether to initiate reproduction, providing insight into how behavior is modified to avoid costly reproductive attempts. Furthermore, our results suggest a temperature constraint that shapes reproductive behavior.

Cost of reproduction, resource quality, and terminal investment in a burying beetle.

We evaluate the cost-of-reproduction hypothesis in the burying beetle Nicrophorus orbicollis and examine how the importance of this trade-off changes as females age (i.e., the terminal-investment hypothesis). These beetles breed on small vertebrate carcasses, which serve as a food resource for them and their offspring. Consistent with the cost-of-reproduction hypothesis, females manipulated to overproduce offspring suffered a reduction in fecundity and life span when compared to controls, although all reproducing females had reduced life spans compared to nonbreeding females. Older females produced larger broods and allocated less of the carcass to their own body mass and a greater proportion to offspring than did younger females. Resource allocation to offspring increased with age. Females given larger carcasses invested more in current reproduction and less in future reproduction than did females given smaller carcasses. Our results provide unconfounded support for both the cost-of-reproduction hypothesis (i.e., current reproduction constrains future reproductive output) and the terminal-investment hypothesis (i.e., the importance of the trade-off between current and future reproduction declines with age such that allocation to current reproduction should increase as females age).

Testes mass in the livebearing fish Brachyrhaphis rhabdophora (Poeciliidae) varies hypoallometrically with body size but not between predation environments.

In this study, we considered potential causes of variation in testis size in the livebearing fish Brachyrhaphis rhabdophora. We evaluated variation in testes mass among individual males and among populations that occupy different selective environments. First, we predicted that small males should allocate more to testes mass than large males (i.e., hypoallometric pattern) based on a sperm competition argument. Second, based on life history theory and associated differences in mortality rates between populations that coexist with many fish predators and those with few predators, we predicted that males in high-predation environments should allocate more to testes mass than males in habitats with few predators. Our results showed that small males allocated proportionally more to testes mass than larger males (slope of testes mass to body mass was hypoallometric). However, there was no effect of predator environment on testes mass independent of body size differences. In this system, size-specific patterns of reproductive allocation in males (hypoallometry) differ from that seen in females (hyperallometry). Allocation to testes mass may respond to differences in mortality rate through selection on body size.

No evidence of nonlinear effects of predator density, refuge availability, or body size of prey on prey mortality rates.

Predator density, refuge availability, and body size of prey can all affect the mortality rate of prey. We assume that more predators will lead to an increase in prey mortality rate, but behavioral interactions between predators and prey, and availability of refuge, may lead to nonlinear effects of increased number of predators on prey mortality rates. We tested for nonlinear effects in prey mortality rates in a mesocosm experiment with different size classes of western mosquitofish (Gambusia affinis) as the prey, different numbers of green sunfish (Lepomis cyanellus) as the predators, and different levels of refuge. Predator number and size class of prey, but not refuge availability, had significant effects on the mortality rate of prey. Change in mortality rate of prey was linear and equal across the range of predator numbers. Each new predator increased the mortality rate by about 10% overall, and mortality rates were higher for smaller size classes. Predator-prey interactions at the individual level may not scale up to create nonlinearity in prey mortality rates with increasing predator density at the population level.

Predation environment affects boldness temperament of neotropical livebearers.

Behavioral traits of individuals are important phenotypes that potentially interact with many other traits, an understanding of which may illuminate the evolutionary forces affecting populations and species. Among the five axes of temperament is the propensity to behave boldly in the presence of a perceived risk. To determine the effect of different predatorial regimes on boldness and fearfulness, we assessed the behavior of individuals in a novel portable swim chamber (i.e., forced open-field test) by Brachyrhaphis rhabdophora (n = 633). We used an information theoretic framework to compare generalized (logistic) linear fixed-effects models of predatorial regime (predator-free [n = 6] and predator [n = 4] sites), sex, and standard length (SL). Fish from predator sites were much more fearful in the novel arena than fish from nonpredator sites. This varied by length, but not by sex. At 48 mm SL, fish from nonpredator sites were 4.9 times more likely to express bold behavior (ambulation) in the novel swim chamber as fish from predator sites. Probabilities of "ambulating" within the swim chamber increased with size for nonpredator sites and decreased with size for predator sites.

Why does it take two to tango? Lifetime fitness consequences of parental care in a burying beetle.

In species that require parental care, each parent can either care for their offspring or leave them in the care of the other parent. For each parent this creates three possible parental care strategies: biparental care, uniparental (male or female) care, and uniparental desertion by either the male or female. The burying beetle, Nicrophorus orbicollis, typically exhibits biparental care of offspring, and thus provides a unique system that allows us to compare the fitness benefits of these parental care strategies in an unconfounded way. In this study, we assess the lifetime fitness of biparental care, uniparental care, and uniparental desertion strategies in both male and female N. orbicollis. Specifically, we tested for increased fitness of the biparental care strategy compared to uniparental care strategies. Second, we test for equality of fitness between uniparental care and uniparental desertion strategies. Surprisingly, biparental care yields lower lifetime fitness for both parents compared to the other two strategies. Also, uniparental care and uniparental desertion strategies yielded equal fitness. The evolution of biparental care in this system is not consistent with the expectation of a mutual fitness benefit. We discuss other potential explanations for the evolution of biparental care in this system.

Differences in Patterns of Reproductive Allocation between the Sexes in Nicrophorus orbicollis.

Organisms are selected to maximize lifetime reproductive success by balancing the costs of current reproduction with costs to future survival and fecundity. Males and females typically face different reproductive costs, which makes comparisons of their reproductive strategies difficult. Burying beetles provide a unique system that allows us to compare the costs of reproduction between the sexes because males and females are capable of raising offspring together or alone and carcass preparation and offspring care represent the majority of reproductive costs for both sexes. Because both sexes perform the same functions of carcass preparation and offspring care, we predict that they would experience similar costs and have similar life history patterns. In this study we assess the cost of reproduction in male Nicrophorus orbicollis and compare to patterns observed in females. We compare the reproductive strategies of single males and females that provided pre- and post-hatching parental care. There is a cost to reproduction for both males and females, but the sexes respond to these costs differently. Females match brood size with carcass size, and thus maximize the lifetime number of offspring on a given size carcass. Males cull proportionately more offspring on all carcass sizes, and thus have a lower lifetime number of offspring compared to females. Females exhibit an adaptive reproductive strategy based on resource availability, but male reproductive strategies are not adaptive in relation to resource availability.

Habitat selection and consumption across a landscape of multiple predators.

Predator community composition can alter habitat quality for prey by changing the strength and direction of consumptive effects. Whether predator community composition also alters prey density via nonconsumptive effects during habitat selection is not well known, but is important for understanding how changes to predator communities will alter prey populations. We tested the hypothesis that predator community composition (presence of caged trout, caged dragonflies, or caged trout + dragonflies) alters colonization of aquatic mesocosms by ovipositing aquatic insects. In a previous experiment in this system, we found a spatial contagion effect, in which insects avoided pools with predators, but only when predator-free pools were isolated (∼5 m away from predator pools). Here, we removed the isolated predator-free pools, allowing us to test whether insects would make fine-scale (∼1 m) oviposition decisions in the absence of preferred isolated pools. We also estimated consumptive effects by allowing predators to feed on colonists for 5 days following colonization. All insects collected after 21 days were dipterans, dominated by Chironomidae. Total colonization, measured as the number of developing larvae after 21 days, was not affected by either predator presence or composition. Consumption was significant in the trout only treatment, reducing larval insect density by 46 ± 37% (mean ± SE). No other predator treatment significantly reduced prey density, although the proportion of chironomid larvae in protective cases increased in response to direct predation from dragonflies, indicating an antipredatory behavioral response. Taken together, these results reveal that predator community composition altered larval survival and behavior, but colonizing females either did not or could not assess these risks across small scales during oviposition.