Rate of evolutionary change in cranial morphology of the marsupial genus Monodelphis is constrained by the availability of additive genetic variation

We tested the hypothesis that the rate of marsupial cranial evolution is dependent on the distribution of genetic variation in multivariate space. To do so, we carried out a genetic analysis of cranial morphological variation in laboratory strains of Monodelphis domestica and used estimates of genetic covariation to analyse the morphological diversification of the Monodelphis brevicaudata species group. We found that within‐species genetic variation is concentrated in only a few axes of the morphospace and that this strong genetic covariation influenced the rate of morphological diversification of the brevicaudata group, with between‐species divergence occurring fastest when occurring along the genetic line of least resistance. Accounting for the geometric distribution of genetic variation also increased our ability to detect the selective regimen underlying species diversification, with several instances of selection only being detected when genetic covariances were taken into account. Therefore, this work directly links patterns of genetic covariation among traits to macroevolutionary patterns of morphological divergence. Our findings also suggest that the limited distribution of Monodelphis species in morphospace is the result of a complex interplay between the limited dimensionality of available genetic variation and strong stabilizing selection along two major axes of genetic variation.     

Quantitative genetic analysis of cranial morphology in the cotton-top (Saguinus oedipus) and saddle-back (S. fuscicollis) tamarins

Patterns of morphological variation play an important role in evolutionary diversification and are critical to an informed interpretation of interspecific differences. When patterns of genetic variation have not diverged substantially, it is possible to reconstruct the differences in selection which gave rise to morphological differences among extant species. Morphological variation patterns are compared between two tamarin species, the cotton-top tamarin (Saguinus oedipus) and the saddle-back tamarin (S. fuscicollis illigeri). Genetic, phenotypic, and environmental variance/covariance and correlation matrices were obtained for a series of 39 cranial characters in each species (cotton-top tamarin, N = 328; saddle-back tamarin, N = 209) and for the species combined using crania from individuals of known genealogical relationship. After accounting for the effects of estimation error on measures of matrix similarity, patterns of phenotypic, genetic, and environmental variation and correlation were found to be very similar across species and among the types of variance within species. Taking the saddle-back tamarins as the standard, cotton-top tamarins have been selected for an enlarged anterior temporalis attachment area and increased facial prognathism. In primates, an enlarged anterior temporalis muscle is associated with incisive food preparation, especially at wide gape.     

A way forward with eco evo devo: an extended theory of resource polymorphism with postglacial fishes as model systems

A major goal of evolutionary science is to understand how biological diversity is generated and altered. Despite considerable advances, we still have limited insight into how phenotypic variation arises and is sorted by natural selection. Here we argue that an integrated view, which merges ecology, evolution and developmental biology (eco evo devo) on an equal footing, is needed to understand the multifaceted role of the environment in simultaneously determining the development of the phenotype and the nature of the selective environment, and how organisms in turn affect the environment through eco evo and eco devo feedbacks. To illustrate the usefulness of an integrated eco evo devo perspective, we connect it with the theory of resource polymorphism (i.e. the phenotypic and genetic diversification that occurs in response to variation in available resources). In so doing, we highlight fishes from recently glaciated freshwater systems as exceptionally well‐suited model systems for testing predictions of an eco evo devo framework in studies of diversification. Studies on these fishes show that intraspecific diversity can evolve rapidly, and that this process is jointly facilitated by (i) the availability of diverse environments promoting divergent natural selection; (ii) dynamic developmental processes sensitive to environmental and genetic signals; and (iii) eco evo and eco devo feedbacks influencing the selective and developmental environments of the phenotype. We highlight empirical examples and present a conceptual model for the generation of resource polymorphism – emphasizing eco evo devo, and identify current gaps in knowledge.     

Which evolutionary processes influence natural genetic variation for phenotypic traits?

Although many studies provide examples of evolutionary processes such as adaptive evolution, balancing selection, deleterious variation and genetic drift, the relative importance of these selective and stochastic processes for phenotypic variation within and among populations is unclear. Theoretical and empirical studies from humans as well as natural animal and plant populations have made progress in examining the role of these evolutionary forces within species. Tentative generalizations about evolutionary processes across species are beginning to emerge, as well as contrasting patterns that characterize different groups of organisms. Furthermore, recent technical advances now allow the combination of ecological measurements of selection in natural environments with population genetic analysis of cloned QTLs, promising advances in identifying the evolutionary processes that influence natural genetic variation.     

RESPONSE TO NATURAL ENVIRONMENTAL HETEROGENEITY: MATERNAL EFFECTS AND SELECTION ON LIFE-HISTORY CHARACTERS AND PLASTICITIES IN MIMULUS GUTTATUS

Recent studies in plant populations have found that environmental heterogeneity and phenotypic selection vary at local spatial scales. In this study, I ask if there is evolutionary change in response to environmental heterogeneity and, if so, whether the response occurs for characters or character plasticities. I used vegetative clones of Mimulus guttatus to create replicate populations of 75 genotypes. These populations were planted into the natural habitat where they differed in mean growth, flowering phenology, and life span. This phenotypic variation was used to define selective environments. There was variation in fitness (flower production) among genotypes across all planting sites and in genotype response to the selective environment. Offspring from each site were grown in the greenhouse in two water treatments. Because each population initially had the same genetic composition, variation in the progeny between selective environments reveals either evolutionary change in response to environmental heterogeneity or environmental maternal effects. Plants from experimental sites that flowered earlier, had shorter life spans and were less productive, produced offspring that had more flowers, on average, and were less plastic in vegetative allocation than offspring of longer-lived plants from high-productivity areas. However, environmental maternal effects masked phenotypic differences in flower production. Therefore, although there was evidence of genetic differentiation in both life-history characters and their plasticities in response to small-scale environmental heterogeneity, environmental maternal effects may slow evolutionary change. Response to local-scale selective regimes suggests that environmental heterogeneity and local variation in phenotypic selection may act to maintain genetic variation.     

Discerning evolutionary processes in patterns of tamarin (genus Saguinus) craniofacial variation

Quantitative genetic theory specifies evolutionary expectations for morphological diversification by genetic drift in a monophyletic clade. If genetic drift is responsible for the evolutionary morphological diversification of a clade, patterns of within- and between-taxon morphological variance/covariance should be proportional. We tested for proportionality of within- and between-species craniofacial morphological variation in 12 species of tamarins (genus Saguinus). We found that within- and between-taxon morphological variations across the entire genus were not proportional, and hence not likely to be due to genetic drift alone. The primary deviation from proportionality is that size and size-related shape in the cranium is more variable relative to other aspects of cranial morphology than expected under genetic drift, suggesting differential size selection between the two major clades, the small-bodied and large-bodied tamarins. Within each of these major clades, most of the interspecific variation is consistent with the pattern expected under genetic drift, although specific contrasts may indicate the involvement of differential selection. Morphological distances among taxa do not correspond very closely to the phylogeny derived from mtDNA. In particular, S. oedipus and S. geoffroyi are very distinct morphologically from the rest of the tamarins, although they are phylogenetically the sister clade to a clade containing S. midas and S. bicolor. Morphological similarity is not a good guide to phylogenetic affinity in the tamarins, especially with regard to deeper nodes in the phylogenetic tree.     

Environmental correlates of geographic divergence in a phenotypic trait: A case study using bat echolocation

Divergence in phenotypic traits may arise from the interaction of different evolutionary forces, including different kinds of selection (e.g., ecological), genetic drift, and phenotypic plasticity. Sensory systems play an important role in survival and reproduction, and divergent selection on such systems may result in lineage diversification. Such diversification could be largely influenced by selection in different environments as a result of isolation by environment (IbE). We investigated this process using geographic variation in the resting echolocation frequency of the horseshoe bat species, Rhinolophus damarensis, as a test case. Bats were sampled along a latitudinal gradient ranging from 16°S to 32°S in the arid western half of southern Africa. We measured body size and peak resting frequencies (RF) from handheld individual bats. Three hypotheses for the divergence in RF were tested: (1) James’ Rule, (2) IbE, and (3) genetic drift through isolation by distance (IbD) to isolate the effects of body size, local climatic conditions, and geographic distance, respectively, on the resting frequency of R. damarensis. Our results did not support genetic drift because there was no correlation between RF variation and geographic distance. Our results also did not support James' Rule because there was no significant relationship between (1) geographic distances and RF, (2) body size and RF, or (3) body size and climatic variables. Instead, we found support for IbE in the form of a correlation between RF and both region and annual mean temperature, suggesting that RF variation may be the result of environmental discontinuities. The environmental discontinuities coincided with previously reported genetic divergence. Climatic gradients in conjunction with environmental discontinuities could lead to local adaptation in sensory signals and directed dispersal such that gene flow is restricted, allowing lineages to diverge. However, our study cannot exclude the role of processes like phenotypic plasticity in phenotypic variation.     

Sex‐specific responses of phenotypic diversity to environmental variation

Identifying the factors generating ecomorphological diversity within species can provide a window into the nascent stages of ecological radiation. Sexual dimorphism is an obvious axis of intraspecific morphological diversity that could affect how environmental variation leads to ecological divergence among populations. In this paper we test for sex‐specific responses in how environmental variation generates phenotypic diversity within species, using the generalist lizard Gallotia galloti on Tenerife (Canary Islands). We evaluate two hypotheses: the first proposes that different environments have different phenotypic optima, leading to shifts in the positions of populations in morphospace between environments; the second posits that the strength of trait‐filtering differs between environments, predicting changes in the volume of morphospace occupied by populations in different environments. We found that intraspecific morphological diversity, provided it is adaptive, arises from both shifts in populations’ position in morphospace and differences in the strength of environmental filtering among environments, especially at high elevations. However, effects were found only in males; morphological diversity of females responded little to environmental variation. These results within G. galloti suggest natural selection is not the sole source of phenotypic diversity across environments, but rather that variation in the strength of, or response to, sexual selection may play an important role in generating morphological diversity in environmentally diverse settings. More generally, disparities in trait–environment relationships among males and females also suggest that ignoring sex differences in studies of trait dispersion and clustering may produce misleading inferences.     

Did natural selection or genetic drift produce the cranial diversification of neotropical monkeys?

A central controversy among biologists is the relative importance of natural selection and genetic drift as creative forces shaping biological diversification (Fisher 1930; Wright 1931). Historically, this controversy has been an effective engine powering several evolutionary research programs during the last century (Provine 1989). While all biologists agree that both processes operate in nature to produce evolutionary change, there is a diversity of opinion about which process dominates at any particular organizational level (from DNA and proteins to complex morphologies). To address this last level, we did a broadscale analysis of cranial diversification among all living New World monkeys. Quantitative genetic models yield specific predictions about the relationship between variation patterns within and between populations that may be used to test the hypothesis that genetic drift is a sufficient explanation for morphological diversification. Diversity at several levels in a hierarchy of taxonomic/phylogenetics relationship was examined from species within genera to families within superfamilies. The major conclusion is that genetic drift can be ruled out as the primary source of evolutionary diversification in cranial morphology among taxa at the level of the genus and above as well as for diversification of most genera. However, drift may account for diversification among species within some Neotropical primate genera, implying that morphological diversification associated with speciation need not be adaptive in some radiations.     

Disruptive selection as a driver of evolutionary branching and caste evolution in social insects

Theory suggests that evolutionary branching via disruptive selection may be a relatively common and powerful force driving phenotypic divergence. Here, we extend this theory to social insects, which have novel social axes of phenotypic diversification. Our model, built around turtle ant (Cephalotes) biology, is used to explore whether disruptive selection can drive the evolutionary branching of divergent colony phenotypes that include a novel soldier caste. Soldier evolution is a recurrent theme in social insect diversification that is exemplified in the turtle ants. We show that phenotypic mutants can gain competitive advantages that induce disruptive selection and subsequent branching. A soldier caste does not generally appear before branching, but can evolve from subsequent competition. The soldier caste then evolves in association with specialized resource preferences that maximize defensive performance. Overall, our model indicates that resource specialization may occur in the absence of morphological specialization, but that when morphological specialization evolves, it is always in association with resource specialization. This evolutionary coupling of ecological and morphological specialization is consistent with recent empirical evidence, but contrary to predictions of classical caste theory. Our model provides a new theoretical understanding of the ecology of caste evolution that explicitly considers the process of adaptive phenotypic divergence and diversification.     

AN ADAPTIVE RADIATION OF FROGS IN A SOUTHEAST ASIAN ISLAND ARCHIPELAGO

Living amphibians exhibit a diversity of ecologies, life histories, and species‐rich lineages that offers opportunities for studies of adaptive radiation. We characterize a diverse clade of frogs (Kaloula, Microhylidae) in the Philippine island archipelago as an example of an adaptive radiation into three primary habitat specialists or ecotypes. We use a novel phylogenetic estimate for this clade to evaluate the tempo of lineage accumulation and morphological diversification. Because species‐level phylogenetic estimates for Philippine Kaloula are lacking, we employ dense population sampling to determine the appropriate evolutionary lineages for diversification analyses. We explicitly take phylogenetic uncertainty into account when calculating diversification and disparification statistics and fitting models of diversification. Following dispersal to the Philippines from Southeast Asia, Kaloula radiated rapidly into several well‐supported clades. Morphological variation within Kaloula is partly explained by ecotype and accumulated at high levels during this radiation, including within ecotypes. We pinpoint an axis of morphospace related directly to climbing and digging behaviors and find patterns of phenotypic evolution suggestive of ecological opportunity with partitioning into distinct habitat specialists. We conclude by discussing the components of phenotypic diversity that are likely important in amphibian adaptive radiations.     

A non‐invasive geometric morphometrics method for exploring variation in dorsal head shape in urodeles: sexual dimorphism and geographic variation in Salamandra salamandra

The study of morphological variation among and within taxa can shed light on the evolution of phenotypic diversification. In the case of urodeles, the dorso‐ventral view of the head captures most of the ontogenetic and evolutionary variation of the entire head, which is a structure with a high potential for being a target of selection due to its relevance in ecological and social functions. Here, we describe a non‐invasive procedure of geometric morphometrics for exploring morphological variation in the external dorso‐ventral view of urodeles' head. To explore the accuracy of the method and its potential for describing morphological patterns we applied it to two populations of Salamandra salamandra gallaica from NW Iberia. Using landmark‐based geometric morphometrics, we detected differences in head shape between populations and sexes, and an allometric relationship between shape and size. We also determined that not all differences in head shape are due to size variation, suggesting intrinsic shape differences across sexes and populations. These morphological patterns had not been previously explored in S. salamandra , despite the high levels of intraspecific diversity within this species. The methodological procedure presented here allows to detect shape variation at a very fine scale, and solves the drawbacks of using cranial samples, thus increasing the possibilities of using collection specimens and alive animals for exploring dorsal head shape variation and its evolutionary and ecological implications in urodeles. J. Morphol. 278:475–485, 2017. © 2017 Wiley Periodicals, Inc.     

The relative contribution of drift and selection to phenotypic divergence: A test case using the horseshoe bats Rhinolophus simulator and Rhinolophus swinnyi

Natural selection and drift can act on populations individually, simultaneously or in tandem and our understanding of phenotypic divergence depends on our ability to recognize the contribution of each. According to the quantitative theory of evolution, if an organism has diversified through neutral evolutionary processes (mutation and drift), variation of phenotypic characteristics between different geographic localities (B) should be directly proportional to the variation within localities (W), that is, B ∝ W. Significant deviations from this null model imply that non‐neutral forces such as natural selection are acting on a phenotype. We investigated the relative contributions of drift and selection to intraspecific diversity using southern African horseshoe bats as a test case. We characterized phenotypic diversity across the distributional range of Rhinolophus simulator (n = 101) and Rhinolophus swinnyi (n = 125) using several traits associated with flight and echolocation. Our results suggest that geographic variation in both species was predominantly caused by disruptive natural selection (B was not directly proportional to W). Evidence for correlated selection (co‐selection) among traits further confirmed that our results were not compatible with drift. Selection rather than drift is likely the predominant evolutionary process shaping intraspecific variation in traits that strongly impact fitness.     

Foraging environment determines the genetic architecture and evolutionary potential of trophic morphology in cichlid fishes

Phenotypic plasticity allows organisms to change their phenotype in response to shifts in the environment. While a central topic in current discussions of evolutionary potential, a comprehensive understanding of the genetic underpinnings of plasticity is lacking in systems undergoing adaptive diversification. Here, we investigate the genetic basis of phenotypic plasticity in a textbook adaptive radiation, Lake Malawi cichlid fishes. Specifically, we crossed two divergent species to generate an F₃ hybrid mapping population. At early juvenile stages, hybrid families were split and reared in alternate foraging environments that mimicked benthic/scraping or limnetic/sucking modes of feeding. These alternate treatments produced a variation in morphology that was broadly similar to the major axis of divergence among Malawi cichlids, providing support for the flexible stem theory of adaptive radiation. Next, we found that the genetic architecture of several morphological traits was highly sensitive to the environment. In particular, of 22 significant quantitative trait loci (QTL), only one was shared between the environments. In addition, we identified QTL acting across environments with alternate alleles being differentially sensitive to the environment. Thus, our data suggest that while plasticity is largely determined by loci specific to a given environment, it may also be influenced by loci operating across environments. Finally, our mapping data provide evidence for the evolution of plasticity via genetic assimilation at an important regulatory locus, ptch1. In all, our data address long‐standing discussions about the genetic basis and evolution of plasticity. They also underscore the importance of the environment in affecting developmental outcomes, genetic architectures, morphological diversity and evolutionary potential.     

The evolution of hominoid cranial diversity: A quantitative genetic approach

Hominoid cranial evolution is characterized by substantial phenotypic diversity, yet the cause of this variability has rarely been explored. Quantitative genetic techniques for investigating evolutionary processes underlying morphological divergence are dependent on the availability of good ancestral models, a problem in hominoids where the fossil record is fragmentary and poorly understood. Here, we use a maximum likelihood approach based on a Brownian motion model of evolutionary change to estimate nested hypothetical ancestral forms from 15 extant hominoid taxa. These ancestors were then used to calculate rates of evolution along each branch of a phylogenetic tree using Lande's generalized genetic distance. Our results show that hominoid cranial evolution is characterized by strong stabilizing selection. Only two instances of directional selection were detected; the divergence of Homo from its last common ancestor with Pan, and the divergence of the lesser apes from their last common ancestor with the great apes. In these two cases, selection gradients reconstructed to identify the specific traits undergoing selection indicated that selection on basicranial flexion, cranial vault expansion, and facial retraction characterizes the divergence of Homo, whereas the divergence of the lesser apes was defined by selection on neurocranial size reduction.     

Sperm size evolution in African greenbuls (Passeriformes: Pycnonotidae)

Sperm morphology is highly diversified across the animal kingdom and recent comparative evidence from passerine birds suggests that postcopulatory sexual selection is a significant driver of sperm evolution. In the present study, we describe sperm size variation among 20 species of African greenbuls and one bulbul (Passeriformes: Pycnonotidae) and analyze the evolutionary differentiation of sperm size within a phylogenetic framework. We found significant interspecific variation in sperm size; with some genera exhibiting relatively long sperm (e.g. Eurillas) and others exhibiting short sperm head lengths (e.g. Phyllastrephus). However, our results suggest that contemporary levels of sperm competition are unlikely to explain sperm diversification within this clade: the coefficients of inter‐male variation (CV_bm) in sperm length were generally high, suggesting relatively low and homogeneous rates of extra‐pair paternity. Finally, in a comparison of six evolutionary or tree transformation models, we found support for both the Kappa (evolutionary change primarily at nodes) and Lambda (lineage‐specific evolutionary rates along branches) models in the evolutionary trajectories of sperm size among species. We therefore conclude that African greenbuls have more variable rates of sperm size evolution than expected from a neutral model of genetic drift. Understanding the evolutionary dynamics of sperm diversification remains a future challenge.     

Location-specific sympatric morphological divergence as a possible response to species interactions in West Virginia Plethodon salamander communities

1. The competitive interactions of closely related species have long been considered important determinants of community composition and a major cause of phenotypic diversification. However, while patterns such as character displacement are well documented, less is known about how local adaptation influences diversifying selection from interspecific competition. 2. We examined body size and head shape variation among allopatric and sympatric populations of two salamander species, the widespread Plethodon cinereus and the geographically restricted P. nettingi. We quantified morphology from 724 individuals from 20 geographical localities throughout the range of P. nettingi. 3. Plethodon nettingi was more robust in cranial morphology relative to P. cinereus, and sympatric localities were more robust relative to allopatric localities. Additionally, there was significantly greater sympatric head shape divergence between species relative to allopatric communities, and sympatric localities of P. cinereus exhibited greater morphological variation than sympatric P. nettingi. 4. The sympatric morphological divergence and increase in cranial robustness of one species (P. nettingi) were similar to observations in other Plethodon communities, and were consistent with the hypothesis of interspecific competition. These findings suggest that interspecific competition in Plethodon may play an important role in phenotypic diversification in this group. 5. The increase in among-population variance in sympatric P. cinereus suggests a species-specific response to divergent natural selection that is influenced in part by other factors. We hypothesize that enhanced morphological flexibility and ecological tolerance allow P. cinereus to more rapidly adapt to local environmental conditions, and initial differences among populations have allowed the evolutionary response of P. cinereus to vary across replicate sympatric locations, resulting in distinct evolutionary trajectories of morphological change.     

Shared and unique features of diversification in Greater Antillean Anolis ecomorphs

Examples of convergent evolution suggest that natural selection can often produce predictable evolutionary outcomes. However, unique histories among species can lead to divergent evolution regardless of their shared selective pressures-and some contend that such historical contingencies produce the dominant features of evolution. A classic example of convergent evolution is the set of Anolis lizard ecomorphs of the Greater Antilles. On each of four islands, anole species partition the structural habitat into at least four categories, exhibiting similar morphologies within each category. We assessed the relative importance of shared selection due to habitat similarity, unique island histories, and unique effects of similar habitats on different islands in the generation of morphological variation in anole ecomorphs. We found that shared features of diversification across habitats were of greatest importance, but island effects on morphology (reflecting either island effects per se or phylogenetic relationships) and unique aspects of habitat diversification on different islands were also important. There were three distinct cases of island-specific habitat diversification, and only one was confounded by phylogenetic relatedness. The other two unique aspects were not related to shared ancestry but might reflect as-yet-unmeasured environmental differences between islands in habitat characteristics. Quantifying the relative importance of shared and unique responses to similar selective regimes provides a more complete understanding of phenotypic diversification, even in this much-studied system.     

DETERMINISM IN THE DIVERSIFICATION OF HISPANIOLAN TRUNK‐GROUND ANOLES (ANOLIS CYBOTES SPECIES COMPLEX)

The evolutionary processes that produce adaptive radiations are enigmatic. They can only be studied after the fact, once a radiation has occurred and been recognized, rather than while the processes are ongoing. One way to connect pattern to process is to study the processes driving divergence today among populations of species that belong to an adaptive radiation, and compare the results to patterns observed at a deeper, macroevolutionary level. We tested whether evolution is a deterministic process with similar outcomes during different stages of the adaptive radiation of Anolis lizards. Using a clade of terrestrial–scansorial lizards in the genus Anolis, we inferred the adaptive basis of spatial variation among contemporary populations and tested whether axes of phenotypic differentiation among them mirror known axes of diversification at deeper levels of the anole radiation. Nonparallel change associated with genetic divergence explains the vast majority of geographic variation. However, we found phenotypic variation to be adaptive as confirmed by convergence in populations occurring in similar habitats in different mountain ranges. Morphological diversification among populations recurs deterministically along two axes of diversification previously identified in the anole radiation, but the characters involved differ from those involved in adaptation at higher levels of anole phylogeny.