Rapid Morphological Divergence Research Articles

Island colonisation leads to rapid behavioural and morphological divergence in Anolis lizards

Island colonisation leads to rapid behavioural and morphological divergence in Anolis lizards

Developmental environment contributes to rapid trait shifts among newly colonized subterranean habitats.

Recent colonization of extreme environments provides unique opportunities to study the early steps of adaptation and the potential for rapid convergent evolution. However, phenotypic shifts during recent colonization may also be due to plasticity in response to changes in the rearing environment. Here, we analyzed a suite of morphological and behavioral traits in paired surface, subterranean, and facultatively subterranean Mexican tetras ( Astyanax mexicanus) from recent introductions in two separate watersheds outside of their native range. We found a variety of phenotypic and behavioral shifts between subterranean and surface populations that are similar to those observed in relatively ancient populations in Mexico. Despite this rapid morphological divergence, we found that most of these trait differences were due to plasticity in response to rearing environments. While most trait assays in common-garden, lab-raised fish indicated that phenotypic shifts in wild fish were the result of plasticity, we also found evidence of genetic control in several traits present in subterranean populations. Interestingly, wall-following behavior, an important subterranean foraging behavior, was greater in lab-born subterranean fish than in lab-born surface fish, suggesting rapid divergence of this trait between subterranean and surface populations. Thus, this study sheds light on the early steps of subterranean evolution, identifies potential rapid behavioral evolution, and suggests that plasticity in traits involving exploratory behavior may facilitate subterranean colonization.

Habitat fragmentation induces rapid divergence of migratory and isolated sticklebacks

AbstractThe adaptive capacity of many organisms is seriously challenged by human-imposed environmental change, which currently happens at unprecedented rates and magnitudes. For migratory fish, habitat fragmentation is a major challenge that can compromise their survival and reproduction. Therefore, it is important to study if fish populations can adapt to such modifications of their habitat. Here, we study whether originally anadromous three-spined stickleback populations (Gasterosteus aculeatus; “migrants”) changed in behavior and morphology in response to human-induced isolation. We made use of a natural field-experiment, where the construction of pumping stations and sluices in the 1970s unintendedly created replicates of land-locked stickleback populations (“resident”) in the Netherlands. For two years, we systematically tested populations of residents and migrants for differences in morphology and behavioral traits (activity, aggressiveness, exploration, boldness, and shoaling) in lab-based assays. We detected differences between migrant and resident populations in virtually all phenotypic traits studied: compared with the ancestral migrants, residents were smaller in size, had fewer and smaller plates and were significantly more active, aggressive, exploratory and bolder, and shoaled less. Despite large ecological differences between 2018 and 2019, results were largely consistent across the two years. Our study shows that human-induced environmental change has led to the rapid and consistent morphological and behavioral divergence of stickleback populations in about 50 generations. Such changes may be adaptive but this remains to be tested.

Rapid morphological divergence following a human-mediated introduction: the role of drift and directional selection

Theory predicts that when populations are established by few individuals, random founder effects can facilitate rapid phenotypic divergence even in the absence of selective processes. However, empirical evidence from historically documented colonisations suggest that, in most cases, drift alone is not sufficient to explain the rate of morphological divergence. Here, using the human-mediated introduction of the silvereye (Zosterops lateralis) to French Polynesia, which represents a potentially extreme example of population founding, we reassess the potential for morphological shifts to arise via drift alone. Despite only 80 years of separation from their New Zealand ancestors, French Polynesian silvereyes displayed significant changes in body and bill size and shape, most of which could be accounted for by drift, without the need to invoke selection. However, signatures of selection at genes previously identified as candidates for bill size and body shape differences in a range of bird species, also suggests a role for selective processes in driving morphological shifts within this population. Twenty-four SNPs in our RAD-Seq dataset were also found to be strongly associated with phenotypic variation. Hence, even under population founding extremes, when it is difficult to reject drift as the sole mechanism based on rate tests of phenotypic shifts, the additional role of divergent natural selection in novel environments can be revealed at the level of the genome.

Influence of invasion history on rapid morphological divergence across island populations of an exotic bird.

There is increasing evidence that exotic populations may rapidly differentiate from those in their native range and that differences also arise among populations within the exotic range. Using morphological and DNA‐based analyses, we document the extent of trait divergence among native North American and exotic Hawaiian populations of northern cardinal (Cardinalis cardinalis). Furthermore, using a combination of historical records and DNA‐based analyses, we evaluate the role of founder effects in producing observed trait differences. We measured and compared key morphological traits across northern cardinal populations in the native and exotic ranges to assess whether trait divergence across the Hawaiian Islands, where this species was introduced between 1929 and 1931, reflected observed variation across native phylogeographic clades in its native North America. We used and added to prior phylogenetic analyses based on a mitochondrial locus to identify the most likely native source clade(s) for the Hawaiian cardinal populations. We then used Approximate Bayesian Computation (ABC) to evaluate the role of founder effects in producing the observed differences in body size and bill morphology across native and exotic populations. We found cardinal populations on the Hawaiian Islands had morphological traits that diverged substantially across islands and overlapped the trait space of all measured native North American clades. The phylogeographic analysis identified the eastern North American clade (C. cardinalis cardinalis) as the most likely and sole native source for all the Hawaiian cardinal populations. The ABC analyses supported written accounts of the cardinal's introduction that indicate the original 300 cardinals shipped to Hawaii were simultaneously and evenly released across Hawaii, Kauai, and Oahu. Populations on each island likely experienced bottlenecks followed by expansion, with cardinals from the island of Hawaii eventually colonizing Maui unaided. Overall, our results suggest that founder effects had limited impact on morphological trait divergence of exotic cardinal populations in the Hawaiian archipelago, which instead reflect postintroduction events.

Ecological opportunity may facilitate diversification in Palearctic freshwater organisms: a case study on hydrobiid gastropods

BackgroundDifferences in species richness among phylogenetic clades are attributed to clade age and/or variation in diversification rates. Access to ecological opportunity may trigger a temporary increase in diversification rates and ecomorphological variation. In addition, lower body temperatures in poikilothermic animals may result in decreasing speciation rates as proposed by the metabolic theory of ecology. For strictly freshwater organisms, environmental gradients within a river continuum, linked to elevation and temperature, might promote access to ecological opportunity and alter metabolic rates, eventually influencing speciation and extinction processes. To test these hypotheses, we investigated the influence of environmental temperature and elevation, as proxies for body temperature and ecological opportunity, respectively, on speciation rates and ecomorphological divergence. As model systems served two closely related gastropod genera with unequal species richness and habitat preferences – Pseudamnicola and Corrosella.ResultsLineage-through-time plots and Bayesian macroevolutionary modeling evidenced that Pseudamnicola species, which typically live in lower reaches of rivers, displayed significantly elevated speciation rates in comparison to the ‘headwater genus’ Corrosella. Moreover, state-dependent speciation models suggested that the speciation rate increased with decreasing elevation, supporting the ecological opportunity hypothesis. In contrast, a significant effect of environmental temperature, as proposed by the metabolic theory of ecology, could not be observed. Disparity-through-time plots, models of ecomorphological evolution, and ancestral habitat estimation showed for Pseudamnicola species rapid morphological divergence shortly after periods of elevational and habitat divergence. In contrast, Corrosella species did not deviate from null models of drift-like evolution.ConclusionOur finding that speciation rates are correlated with elevation and ecomorphological disparity but not with environmental temperatures suggests that differences in ecological opportunity may have played a key role in Corrosella and Pseudamnicola diversifications. We propose that Pseudamnicola lineages experienced higher ecological opportunity through dispersal to new locations or habitats in lowlands, which may explain the increase in speciation rates and morphological change. In contrast, the evolution of Corrosella in headwaters is likely less facilitated by the environment and more by non-ecological processes.

Rapid morphological divergence in two closely related and co-occurring species over the last 50 years

We studied morphological variation in two closely related and ecologically similar species of mice of the genus Peromyscus, the deer mouse (P. maniculatus) and white-footed mouse (P. leucopus), over the last 50 years in Southern Quebec. We found that contemporary populations of the two species are distinct in morphology and interpret this differentiation as a reflection of resource partitioning, a mechanism favouring their local coexistence. While there was no size trend, geographic or temporal, both species displayed a concomitant change in the shape of their skull over the last 50 years, although this change was much more apparent in the white-footed mouse. As a result, the two species diverged over time and became more distinct in their morphology. The observed changes in morphology are large given the short time scale. During this period, there was also a shift in abundance of the two species in Southern Quebec, consistent with the northern displacement of the range of the white-footed mouse in the last 15 years. Our study thus reports the changes in morphology of two co-occurring mammal species that were accompanied by changes in distribution and local abundance, potentially in response to rapid climate change.

Rapid morphological divergence of cultured cod of the northwest Atlantic from their source population

The performance of aquaculture escapees in the wild depends in part on how their morphology differs from that of wild fish. We compared farmed Atlantic cod Gadus morhua morphology to that of wild cod from the same ancestral population. Traditional and geometric morphometrics showed that farmed cod had relatively smaller fins, heads, eyes, and jaws than wild cod for a given size. Conversely, drumming muscle size and metrics of body and liver condition were greater in farmed fish. As the observed differences are likely due to phenotypic plasticity, their fitness consequences for escaped farmed fish may be transient.

Dramatic niche shifts and morphological change in two insular bird species.

Colonizations of islands are often associated with rapid morphological divergence. We present two previously unrecognized cases of dramatic morphological change and niche shifts in connection with colonization of tropical forest-covered islands. These evolutionary changes have concealed the fact that the passerine birds madanga, Madanga ruficollis, from Buru, Indonesia, and São Tomé shorttail, Amaurocichla bocagii, from São Tomé, Gulf of Guinea, are forest-adapted members of the family Motacillidae (pipits and wagtails). We show that Madanga has diverged mainly in plumage, which may be the result of selection for improved camouflage in its new arboreal niche, while selection pressures for other morphological changes have probably been weak owing to preadaptations for the novel niche. By contrast, we suggest that Amaurocichla's niche change has led to divergence in both structure and plumage.

Rapid morphological divergence of a stream fish in response to changes in water flow

Recent evidence indicates that evolution can occur on a contemporary time scale. However, the precise timing and patterns of phenotypic change are not well known. Reservoir construction severely alters selective regimes in aquatic habitats due to abrupt cessation of water flow. We examined the spatial and temporal patterns of evolution of a widespread North American stream fish ( Pimephales vigilax ) in response to stream impoundment. Gross morphological changes occurred in P. vigilax populations following dam construction in each of seven different rivers. Significant changes in body depth, head shape and fin placement were observed relative to fish populations that occupied the rivers prior to dam construction. These changes occurred over a very small number of generations and independent populations exhibited common responses to similar selective pressures. The magnitude of change was observed to be greatest in the first 15 generations post-impoundment, followed by continued but more gradual change thereafter. This pattern suggests early directional selection facilitated by phenotypic plasticity in the first 10–20 years, followed by potential stabilizing selection as populations reached a new adaptive peak (or variation became exhausted). This study provides evidence for rapid, apparently adaptive, phenotypic divergence of natural populations due to major environmental perturbations in a changing world.

Anthropogenic habitat alteration induces rapid morphological divergence in a native stream fish.

Anthropogenic habitat alteration creates novel environments that can alter selection pressures. Construction of reservoirs worldwide has disturbed riverine ecosystems by altering biotic and abiotic environments of impounded streams. Changes to fish communities in impoundments are well documented, but effects of those changes on native species persisting in reservoirs, which are presumably subjected to novel selective pressures, are largely unexplored. I assessed body shape variation of a native stream fish in reservoir habitats and streams from seven reservoir basins in the Central Plains of the USA. Body shape significantly and consistently diverged in reservoirs compared with stream habitats within reservoir basins; individuals from reservoir populations were deeper-bodied and had smaller heads compared with stream populations. Individuals from reservoir habitats also exhibited lower overall shape variation compared with stream individuals. I assessed the contribution of genotypic divergence and predator-induced phenotypic plasticity on body shape variation by rearing offspring from a reservoir and a stream population with or without a piscivorous fish. Significant population-level differences in body shape persisted in offspring, and both populations demonstrated similar predator-induced phenotypic plasticity. My results suggest that, although components of body shape are plastic, anthropogenic habitat modification may drive trait divergence in native fish populations in reservoir-altered habitats.

A molecular characterization of the charismatic Faroe house mouse

Faroe house mice are a ‘classic’ system of rapid and dramatic morphological divergence highlighted by J. S. Huxley during the development of the Modern Synthesis. In the present study, we characterize these charismatic mice using modern molecular techniques, examining specimens from all Faroe islands occupied by mice. The aims were to classify the mice within the modern house mouse taxonomy (i.e. as either Mus musculus domesticus or Mus musculus musculus) using four molecular markers and a morphological feature, and to examine the genetic diversity and possible routes of colonization using mitochondrial (mt) control region DNA sequences and microsatellite data (15 loci). Mice on the most remote islands were characterized as M. m. domesticus and exhibited exceptionally low genetic diversity, whereas those on better connected islands were more genetically diverse and had both M. m. musculus and M. m. domesticus genetic elements, including one population which was morphologically M. m. musculus-like. The mtDNA data indicate that the majority of the mice had their origins in south-western Norway (or possibly southern Denmark/northern Germany), and probably arrived with the Vikings, earlier than suggested by Huxley. The M. m. musculus genetic component appears to derive from recent mouse immigration from Denmark. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102, 471–482.

Eastern fox squirrel (Sciurus niger) lacks phylogeographic structure: recent range expansion and phenotypic differentiation

The eastern fox squirrel (Sciurus niger) occurs naturally over most of eastern North America. The striking patterns of geographic variation in size and coat color displayed by this species are consistent with a hypothesis of southward range contraction and isolation in 2 refugia (in Texas and Florida) during the Last Glacial Maximum, followed by northward range expansion after the glaciers receded. Similar hypotheses have been proposed to explain the patterns in phylogeographic structure exhibited by many plants and animals in eastern North America. We analyzed DNA sequence variation in a 402–base-pair segment of the mitochondrial cytochrome-b gene in populations throughout the species’ range. Despite our broad geographic sampling, we failed to detect any phylogeographic structure. Unique haplotypes differed from high-frequency haplotypes by only 1 or 2 base pairs, producing a starlike phylogeny of haplotypes. Genetic variation within populations and the species as a whole was characterized by high haplotype diversity and low nucleotide diversity. Taken together, our data indicate that the eastern fox squirrel underwent a rapid range expansion and rapid morphological divergence within the past 14,000 years. DOI: 10.1644/09-MAMM-A-266.1.

Evolutionary genetics of genital size and lateral asymmetry in the earwig Euborellia plebeja (Dermaptera: Anisolabididae)

Male genitalia show several evolutionary characteristics, including rapid morphological divergence between closely related species and low within-species phenotypic variability. In addition, genital asymmetry is widespread despite the essentially bilaterally symmetric external morphology of insects. Several hypotheses, such as sexual selection and lock-and-key hypotheses, have been proposed to explain these characteristics of genital evolution. Although these hypotheses provide different predictions about the genetic basis of variation in genitalia, detailed quantitative genetic studies have been conducted in only three insect taxa: heteropterans, dung beetles (Scarabaeidae), and drosophilid flies. For an anisolabidid earwig, Euborellia plebeja, characterized by paired elongated intromittent organs, we estimated the heritabilities and genetic correlations of genital laterality, size of genitalia, and body size. No statistically significant additive genetic, dominance, maternal, or common environmental effects were detected for genital laterality (readiness to use either the left or the right intromittent organ). This result lends further support to the general rule that the direction of antisymmetric variations is randomly determined by non-genetic factors. Irrespective of the restricted phenotypic variation in genitalia compared with body size (allometric slope < 1), as observed in previous studies for other insects, these two traits showed a similar level of genetic variation, measured as the narrow sense heritability (h2) and the coefficient of additive genetic variation (CVA). Comparison suggests the causes of interspecific differences in genetic variability/correlation structures were developmental processes (holo- or hemimetabolous) and/or mode of sexual selection. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101, 103–112.

Stable isotope analysis to examine possible diet-morphology relationships among Red-whiskered Bulbuls introduced on Réunion Island

A recent study on the introduced Red-whiskered Bulbul Pycnonotus jocosus on Réunion Island has highlighted the existence of rapid morphological divergence in bill size between the leeward and windward sides of the island. The hypothesis that diet could explain such geographical variation was explored by means of stable isotope analysis (C and N) on bird tissues. We found no evidence of geographical differences in δ15N and δ13C in muscle and feather tissues of birds collected on both sides of the island, despite morphological differences. Correlations between wing length, tail length and δ15N in tissues suggested that bigger birds could benefit from greater feeding opportunities on insects. However, stable isotope ratios in bird tissues marginally explained variation in bill size, indicating that diet specialisation may not be the major cause for morphological divergence among Red-whiskered Bulbuls on Réunion Island.

400 years for long-distance dispersal and divergence in the northern Atacama desert – Insights from the Huaynaputina pumice slopes of Moquegua, Peru

The Huaynaputina eruption (1600 AD, Moquegua, S Peru) in the northern Atacama Desert denuded the Omate area of all vegetation and deposited deep pumice layers. Data on the flora, climate and soil characteristics of these slopes near Omate at 1600–2600 m a.s.l. are provided. Fifty-nine angiosperm species established themselves on the pumice slopes in the past ca. 400 years, with the bulk of the small and herbaceous species and several species new records for Peru. Three Omate sites were sampled in both a dry and a wet year and species numbers differed widely (14 versus 45 spp.). Among areas compared floristic composition is most similar to the Lomas de Tacna, and has less in common with geographically closer Lomas or Sierra formations. Nine species represent highly disjunct populations (200–>700 km) from their nearest known living populations in central Peru, Chile, or Argentina/Bolivia and appear to have reached the area via long-distance dispersal. Abiotic conditions may have played an important role in limiting the establishment of species from the neighboring vegetation. Four taxa on the pumice slopes show clear morphological differences to populations elsewhere, two of them may represent neoendemics of the Omate pumice, indicating rapid morphological divergence.

Escape to Alcatraz: evolutionary history of slender salamanders (Batrachoseps) on the islands of San Francisco Bay

BackgroundIsland populations are excellent model systems for studies of phenotypic, ecological and molecular evolution. In this study, molecular markers of mitochondrial and nuclear derivation were used to investigate the evolution, structure and origin of populations of the California slender salamander (Batrachoseps attenuatus) inhabiting the six major islands of San Francisco Bay, formed following the rising of sea level around 9,000 years ago.ResultsThere was a high degree of congruence in the results of analyses of nucleotide and allozyme data, both of which strongly support the hypothesis that, for the majority of the islands, salamanders are descended from hilltop populations that became isolated with the formation of the Bay ca. 9,000 years ago. There are two exceptions (Alcatraz and Yerba Buena) where the evidence suggests that salamander populations are wholly or in part, the result of anthropogenic introductions.Comparison of the molecular data and the interpretations drawn therefrom with an earlier morphological study of many of the same salamander populations show some of the same evolutionary trends.ConclusionIn spite of marked differences between the evolutionary rates of the two kinds of molecular markers, both indicate distinctive and similar patterns of population structure for B. attenuatus in the San Francisco Bay Area and its islands. With the two noted exceptions, it is clear that most island populations were established prior to the 9,000 years since the formation of the Bay. Results of coalescence-based analyses suggest that for most island populations the mtDNA lineages from which they were derived date from the Pleistocene.It can be said that, based on observed values of genetic diversity, the last 9,000 years of evolution on these islands have been characterized by relative stability, with the occasional extinction of some haplotypes or alleles that were formerly shared between island and mainland populations but overall maintaining high levels of variation (with the exception of Alcatraz). In contrast, there is some evidence for rapid morphological changes between populations in some islands and their closest mainland counterparts. This pattern of rapid morphological divergence (e. g., resulting from founder effects) is similar to that observed in other studies about recent colonization of island habitats.

Rapid morphological divergence of introduced Red‐whiskered BulbulsPycnonotus jocosusin contrasting environments

New environmental conditions may impact on behaviour and morphology, and consequently affect population dynamics. Rapid response to new conditions is likely to be a key factor in species introduction success. The Red‐whiskered BulbulPycnonotus jocosusis an Asian species which, following accidental introduction only 30 years ago, has colonized the two climatically and ecologically contrasting sides of the island of Réunion in the Indian Ocean. We assessed the degree of morphological divergence of mature birds in 11 non‐seasonal and three seasonal characters, in windward and leeward sites. Our study showed (1) that sexual dimorphism existed, (2) that when sexual dimorphism is controlled, nine non‐seasonal characters differed significantly between windward and leeward sites, (3) that these non‐seasonal characters define groups of geographically proximal sites, especially in males, and (4) that classification according to the most indicative character, the bill, also clearly separated birds from windward and leeward sites. These results indicate very rapid morphological divergence, particularly in bill size, in an introduced bird species in fewer than ten generations. We suggest that differences in diet could partly explain this variability.

Rapid Morphological Changes in Threespine Stickleback, Gasterosteus aculeatus, in Freshwater

Freshwater and marine threespine stickleback, Gasterosteus aculeatus, differ remarkably in armour plate number and body shape, although differences in other morphological characters are also common. Most freshwater populations have apparently evolved after isolation of marine sticklebacks in freshwater. After colonisation of freshwater habitats, they show rapid morphological changes and associated genetic isolation within as few as eight generations. I transferred fish from marine tide pools to two isolated freshwater ponds, differing in habitat characteristics, at the beginning of the breeding season, when females had ripe ovaries and males had breeding coloration. The first generation fish that I sampled from the ponds had significantly fewer armour plates than their marine ancestors and differed in shape. I also found some significant differences between fish sampled from the larger pond and those from a smaller, adjacent pond. This extremely rapid morphological divergence suggests that either the marine sticklebacks were highly phenotypically plastic or that there was very strong natural selection acting on the first generation within freshwater habitats.

Radiating in a river: systematics, molecular genetics and morphological differentiation of viviparous freshwater gastropods endemic to the Kaek River, central Thailand (Cerithioidea, Pachychilidae)

Speciation in the context of adaptive radiation is regarded as a key process in the creation of biodiversity. While several lacustrine species flocks provide ideal models for elucidating the underlying evolutionary mechanisms, riverine radiations are both rarely known and studied. The Kaek River, a third-order tributary of the Nan River and Chao Praya drainage in central Thailand, harbours an exceptional endemic species assemblage of morphologically distinct, viviparous pachychilid gastropods. Our systematic revision, combining a morphological and molecular genetics approach, reveals the sympatric existence of at least seven species of the genus Brotia that is widespread in rivers of South-east Asia where usually only two species at the most coexist. At eight locations along a 100-kilometre stretch of the Kaek River, we found the syntopic occurrence of two to three species that are separated by specific habitat preferences and exhibit trophic specialization in their radula morphology. Phylogenetic analyses (using MP, NJ, ML and Bayesian inference statistics) of partial COI and 16S sequence data of 17 samples from six species occurring sympatrically and parapatrically, respectively, in the Kaek River drainage (plus the type species B. pagodula as outgroup) indicate monophyly of all these endemic species. Brotia solemiana, which also occurs in the Loei River, a tributary of the Mekong drainage system, was found to be sister to all other Kaek River pachychilids. The distinctive morphotypes, proposed here to represent biospecies, do not show high levels of genetic variation consistent with long periods of reproductive isolation. This suggests a relatively recent origin of this intrariverine radiation and rapid morphological divergence in the Kaek River Brotia. Recent diversification combined with ecological separation and trophic specialization parallels conditions found, albeit on a more specious level, in the lacustrine species flock of the closely related pachychilid genus Tylomelania, which is endemic to ancient lakes on the Indonesian island of Sulawesi. We discuss and compare the allopatric and ecological aspects of speciation in this unique riverine radiation and outline a putative historical biogeography of the Kaek River species, employing the most recent geological and palaeohydrological data for Thailand.