Superfetation is the ability of females to simultaneously carry multiple broods of embryos, with each brood at a different developmental stage. Matrotrophy is the post-fertilization maternal provisioning of nutrients to developing embryos throughout gestation. Several studies have demonstrated that, in viviparous fishes, superfetation and matrotrophy have evolved in a correlated way, such that species capable of bearing several simultaneous broods also exhibit advanced degrees of post-fertilization provisioning. The adaptive value of the concurrent presence of both reproductive modes may be associated with the production of larger newborns, which in turn may result in enhanced offspring fitness. In this study, we tested two hypotheses: (1) species with superfetation and moderate or extensive matrotrophy give birth to larger offspring compared to species without superfetation or matrotrophy; (2) species with higher degrees of superfetation and matrotrophy (i.e. more simultaneous broods and increased amounts of post-fertilization provisioning) give birth to larger offspring compared to species with relatively low degrees of superfetation and matrotrophy (i.e. fewer simultaneous broods and lesser amounts of post-fertilization provisioning). Using different phylogenetic comparative methods and data on 44 species of viviparous fishes of the family Poeciliidae, we found a lack of association between offspring size and the combination of superfetation and matrotrophy. Therefore, the concurrent presence of superfetation and moderate or extensive matrotrophy has not facilitated the evolution of larger offspring. In fact, these traits have evolved differently. Superfetation and matrotrophy have accumulated gradual changes that largely can be explained by Brownian motion, whereas offspring size has evolved fluidly, experiencing changes that likely resulted from selective responses to the local conditions.
A hierarchy is an abstract organizational model of inter-level relationships among entities. When isomorphic with nature, hierarchies are useful for organizing and manipulating our knowledge. Hierarchies have been used in biological systematics to represent several distinct, but interrelated, facets of the evolution of life with different organizational properties, and these distinctions have been confused by the rubric «the hierarchy of life». Evolution, as descent with modification, is inherently dualistic. The organizational structure of a hierarchy can be used to represent dualistic properties as inter-level relationships. Cladistics is monistic, with a singular focus on patterns of descent. Descent has conceptual priority over modification, but the organizational relationship is not exclusive. «Cladistic classification» is an oxymoron because cladistics lacks the class concepts needed to construct a classification, a point recognized by those who suggest abandoning Linnaean classification in favour of a newly devised monophyletic systematization. Cladistic analysis of descent can be supplemented with an analysis of modification that provides the class concepts needed to construct an evolutionary/phylogenetic classification. When a strong monophyletic pattern of modification is detected (in addition to its monophyletic pattern of descent), the criterion of subsequent modification provides the basis for formally recognizing a certain monophyletic group at a given rank, as opposed to a group that is one node more inclusive or one node less. The criterion of subsequent modification also permits detection of strong paraphyletic patterns of modification, when they exist. By setting standards of evidence needed to recognize paraphyletic groups, one concomitantly strengthens the basis for formally recognizing selective monophyletic groups.Copyright 1998 The Linnean Society of London
Sexual selection through female choice has driven the evolution of some of the most elaborate signalling behaviours in animals. These displays often require specialized morphological adaptations and may incorporate signals in multiple sensory modalities. Visual and acoustic signals are often precisely choreographed in temporally structured courtship performances, though the precise mechanics of such signalling behaviours are often enigmatic. We find that riflebirds (genus Ptiloris)-a bird of paradise clade-achieve their remarkable display postures by hyperextending the wrist joint, vastly exceeding the maximal wrist extension capabilities of any other known bird. Using video collected in the field, we then show that this hypermobility is required for a sonation unique to riflebirds, and find that the yellow interior of the mouth is displayed in the dynamic phase of display. As this sonation cannot be produced when the mouth is exposed, it represents a mechanical constraint to signal design. Finally, we used a large morphometric dataset to describe patterns of sexual dimorphism in wing length across diverse bird of paradise species, and find evidence of sexual selection for large and structurally modified wings used in riflebird displays. Our study highlights nuanced choreographic differences in the display behaviours of different riflebird species, and sheds light on the intricate design features of sexual signals in this fascinating taxon.
Interdemic selection, inbreeding and highly structured populations have been invoked to explain the evolution of cooperative social behaviour in the otherwise solitary and cannibalistic spiders. The family Eresidae consists of species ranging from solitary and intermediate subsocial to species exhibiting fully cooperative social behaviour. In this study we, in a hierarchical analysis, investigated relatedness of putative family clusters, inbreeding and population genetic structure of the subsocial spider Eresus cinnaberinus. Five hierarchical levels of investigation ranging from large scale genetic structure (distances of 250 and 50 km level 1 and 2) over microgeographic structure (20 km2 and 4 km2, level 3 and 4) to a single hill transect of 200 m (level 5) were performed. The purpose of level 5 was two-fold: (1) to investigate the relatedness of putative family groups, and (2) to evaluate the influence of both family living and sampling design on higher level estimates. Relatedness estimates of putative family groups showed an average relatedness of R=0.26. There was no indication of inbreeding. In contrast to social spiders, genetic variation was abundant, Heapproximately0.10. The population genetic structure was intermediate between social and asocial spiders. Genetic variance increased continually across hierarchical levels. Family structured neighbourhoods biased differentiation estimates among level 5 samples (FST=0.04) and level 3 and 4 samples (0.07<FST<0.18), and apparent inbreeding among level 3 and 4 samples, FIS>0, was caused by disjunct sampling from separate neighbourhoods. Larger scale samples were highly differentiated 0.12<FST<0.26, depending on level and sampling design. Due to a distance effect family living did not influence estimates of the higher level 1. Although the dispersing sex among social spiders and the subsocial E. cinnebarinus differ, females versus males, female behaviour of both sociality classes lead to high genetic variance.Copyright 1998 The Linnean Society of London
The slender filefish is a master of adaptive camouflage and can change its appearance within 1-3 seconds. Videos and photographs of this animal's cryptic body patterning and behavior were collected in situ under natural light on a Caribbean coral reef. We present an ethogram of body patterning components that includes large- and small-scale spots, stripes and bars that confer a variety of cryptic patterns amidst a range of complex backgrounds. Field images were analyzed to investigate two aspects of camouflage effectiveness: (i) the degree of color resemblance between animals and their nearby visual stimuli and (ii) the visibility of each fish's actual body outline versus its illusory outline. Most animals more closely matched the color of nearby visual stimuli than that of the surrounding background. Three-dimensional dermal flaps complement the melanophore skin patterns by enhancing the complexity of the fish's physical skin texture to disguise its actual body shape, and the morphology of these structures was studied. The results suggest that the body patterns, skin texture, postures and swimming orientations putatively hinder both the detection and recognition of the fish by potential visual predators. Overall, the rapid speed of change of multiple patterns, color blending with nearby backgrounds, and the physically complicated edge produced by dermal flaps effectively camouflage this animal among soft corals and macroalgae in the Caribbean Sea.
The insects with the longest proboscis in relation to body length are the nectar-feeding Nemestrinidae. These flies represent important pollinators of the South African flora and feature adaptations to particularly long-tubed flowers. The present study examined the morphology of the extremely long and slender mouthparts of Nemestrinidae for the first time. The heavily sclerotized tubular proboscis of flies from the genus Prosoeca is highly variable in length. It measures 20-47 mm in length and may exceed double the body length in some individuals. Proximally, the proboscis consists of the labrum-epipharynx unit, the laciniae, the hypopharynx, and the labium. The distal half is composed of the prementum of the labium, which solely forms the food tube. In adaptation to long-tubed and narrow flowers, the prementum is extremely elongated, bearing the short apical labella that appear only to be able to spread apart slightly during nectar uptake. Moving the proboscis from resting position under the body to a vertical feeding position is accomplished in particular by the movements of the laciniae, which function as a lever arm. Comparisons with the mouthparts of other flower visiting flies provide insights into adaptations to nectar-feeding from long-tubed flowers.
The foxes at Novosibirsk, Russia, are the only population of domesticated foxes in the world. These domesticated foxes originated from farm-bred silver foxes (Vulpes vulpes), whose genetic source is unknown. In this study we examined the origin of the domesticated strain of foxes and two other farm-bred fox populations (aggressive and unselected) maintained in Novosibirsk. To identify the phylogenetic origin of these populations we sequenced two regions of mtDNA, cytochrome b and D-loop, from 24 Novosibirsk foxes (8 foxes from each population) and compared them with corresponding sequences of native red foxes from Europe, Asia, Alaska and Western Canada, Eastern Canada, and the Western Mountains of the USA. We identified seven cytochrome b - D-loop haplotypes in Novosibirsk populations, four of which were previously observed in Eastern North America. The three remaining haplotypes differed by one or two base change from the most common haplotype in Eastern Canada. Φ(ST) analysis showed significant differentiation between Novosibirsk populations and red fox populations from all geographic regions except Eastern Canada. No haplotypes of Eurasian origin were identified in the Novosibirsk populations. These results are consistent with historical records indicating that the original breeding stock of farm-bred foxes originated from Prince Edward Island, Canada. Mitochondrial DNA data together with historical records indicate two stages in the selection of domesticated foxes: the first includes captive breeding for ~50 years with unconscious selection for behaviour; the second corresponds to over 50 further years of intensive selection for tame behaviour.
Multilocus electrophoretic methods and microcomplement fixation comparisons of serum albumin are used to assess phylogenetic relationships among species of uropeltid snakes, to infer aspects of their population biology and biogeography, and to evaluate their relationships to other primitive snakes (Henophidia). There is very good agreement between phylogenetic inferences derived from the electrophoretic data and those derived from the albumin immunological data. Protein variation detected by electrophoresis is relatively high among 17 operational taxonomic units (OTUs) examined. The mean number of alleles per locus (5.1 across all OTUs), levels of polymorphism (25% of loci), and heterozygosity (4-6%), are typical of, or greater than, values reported for other snakes. Species of uropeltids are genetically highly differentiated, as measured by genetic distances (lowest interspecific Nei's unbiased genetic distances, 0.22-0.27 among several Sri Lankan species; 2.3 between Teretrurus of India and other uropeltines). The phylogenetic tree most consistent with both the immunological and electrophoretic data shows uropeltines from Sri Lanka to be monophyletic, but the Indian species are paraphyletic with respect to those from Sri Lanka. Rhinophis travancoricus of India is inferred to be the sister taxon to the Sri Lankan radiation. As the genera are presently understood, neither Rhinophis nor Uropeltis appears to be monophyletic. A biogeographic scenario derived from the phylogenetic hypothesis suggests an early diversification of uropeltids in India, followed by a single invasion into the lowlands of Sri Lanka. Subsequent evolution on Sri Lanka resulted in occupation of montane biotopes. Cylindrophis is the sister group to uropeltines and is considered a member of the Uropeltidae. The immunological data indicate no phylogenetic association between uropeltids and other 'anilioid' taxa, specifically Anilius, Loxocemus or Xenopeltis, although we cannot rule out a very remote relationship. We specifically reject the hypothesis that uropeltines and scolecophidians form a clade relative to henophidians. High levels of genetic variation and a trend toward negative FIS values for polymorphic loci in three populations suggest generally large effective population sizes and outbreeding in these species. The niche-width variation hypothesis for allozyme loci is not supported by the uropeltid data. In comparison to other vertebrates, the relationship between Nei's genetic distance and albumin immunological distance in uropeltids suggests either conservative albumin evolution or strong differentiation at electrophoretic loci.
The brown bear (Ursus arctos) is an iconic carnivoran species of the Northern Hemisphere. Its population history has been studied extensively using mitochondrial markers, which demonstrated signatures of multiple waves of migration, arguably connected with glaciation periods. Among Eurasian brown bears, Siberian populations remain understudied. We have sequenced complete mitochondrial genomes of four ancient (~4.5-40 kya) bears from South Siberia and 19 modern bears from South Siberia and the Russian Far East. Reconstruction of phylogenetic relationships between haplotypes and evaluation of modern population structure have demonstrated that all the studied samples belong to the most widespread Eurasian clade 3. One of the ancient haplotypes takes a basal position relative to the whole of clade 3; the second is basal to the haplogroup 3a (the most common subclade), and two others belong to clades 3a1 and 3b. Modern Siberian bears retain at least some of this diversity; apart from the most common haplogroup 3a, we demonstrate the presence of clade 3b, which was previously found mainly in mainland Eurasia and Northern Japan. Our findings highlight the importance of South Siberia as a refugium for northern Eurasian brown bears and further corroborate the hypothesis of several waves of migration in the Pleistocene.
Many species of fish display morphological divergence between individuals feeding on macroinvertebrates associated with littoral habitats (benthic morphotypes) and individuals feeding on zooplankton in the limnetic zone (limnetic morphotypes). Threespine stickleback (Gasterosteus aculeatus L.) have diverged along the benthic-limnetic axis into allopatric morphotypes in thousands of populations and into sympatric species pairs in several lakes. However, only a few well known populations have been studied because identifying additional populations as either benthic or limnetic requires detailed dietary or observational studies. Here we develop a Fisher's linear discriminant function based on the skull morphology of known benthic and limnetic stickleback populations from the Cook Inlet Basin of Alaska and test the feasibility of using this function to identify other morphologically divergent populations. Benthic and limnetic morphotypes were separable using this technique and of 45 populations classified, three were identified as morphologically extreme (two benthic and one limnetic), nine as moderately divergent (three benthic and six limnetic) and the remaining 33 populations as morphologically intermediate. Classification scores were found to correlate with eye size, the depth profile of lakes, and the presence of invasive northern pike (Esox lucius). This type of classification function provides a means of integrating the complex morphological differences between morphotypes into a single score that reflects the position of a population along the benthic-limnetic axis and can be used to relate that position to other aspects of stickleback biology.
The Apennine Mountains in Italy are an important biogeographical region and of particular interest in phylogeographical research, because they have been a refugium during Pleistocene glaciation events for numerous European species. We performed a genetic study on the Eurasian bark beetle Pityogenes chalcographus (Linnaeus, 1760), focusing on two Apennine (Italian) and two Central European (Austrian) locations to assess the influence of the Apennines in the evolutionary history of the beetle, particularly during the Pleistocene. We analysed a part of the mitochondrial COI gene and a set of 5470 informative genome-wide markers to understand its biogeography. We found 75 distinct mitochondrial haplotypes, which are structured in three main clades. In general, the Apennine locations harbour a higher number of mitochondrial clades than Central European sites, with one specific clade exclusively detected in the Apennines. Analysis of our genome-wide, multi-locus dataset reveals a clustering of P. chalcographus by geography, with Italian individuals clearly separated from Austrian samples. Our data highlight the significance of the Apennines for the genetic diversity of P. chalcographus and support the hypothesis that this area was an important refugium during unfavourable conditions in the Pleistocene. We discuss additional life-history traits and processes that shaped the evolution of this widespread beetle.
Morphological adaptations in the jaws of snakes directly enable many elements of their unique feeding ecology, including the ability to swallow large prey items whole. However, macroevolutionary trends between snake dietary ecology and jaw system morphology have yet to be investigated with dense sampling across a broad phylogenetic scale. We used computerized tomography data and phylogenetic comparative methods to explore the evolution of two functionally important jaw traits, relative quadrate length (RQL) and jaw-closing mechanical advantage (MA), across nearly 600 species of colubroid snakes. While relative prey bulk explained observed patterns of quadrate length evolution largely on its own, both relative prey bulk and relative prey mass influenced the evolution of mechanical advantage. Additionally, there was a weak but significant inverse relationship between RQL and MA. We suggest that selection for maintaining a large gape has largely co-opted the force-velocity trade-off to become the primary driver of jaw system evolution in snakes. Our results highlight the significance of macrostomy as an important innovation in the evolutionary history of snakes and provide new insights into the macroevolutionary relationship between ecology and phenotype in this diverse global radiation.
Sexual traits vary tremendously in static allometry. This variation may be explained in part by body size-related differences in the strength of selection. We tested this hypothesis with in two populations of vervet monkeys, using estimates of the level of condition dependence for different morphological traits as a proxy for body size-related variation in the strength of selection. In support of the hypothesis, we found that the steepness of allometric slopes increased with the level of condition dependence. One trait of particular interest, the penis, had shallow allometric slopes and low levels of condition dependence, in agreement with one of the most consistent patterns yet detected in the study of allometry, that of genitalia exhibitting shallow allometries.
An assessment of the anatomical costs of extremely long proboscid mouthparts can contribute to the understanding of the evolution of form and function in the context of insect feeding behaviour. An integrative analysis of expenses relating to an exceptionally long proboscis in butterflies includes all organs involved in fluid feeding, such as the proboscis plus its musculature, sensilla, and food canal, as well as organs for proboscis movements and the suction pump for fluid uptake. In the present study, we report a morphometric comparison of derived long-tongued (proboscis approximately twice as long as the body) and short-tongued Riodinidae (proboscis half as long as the body), which reveals the non-linear scaling relationships of an extremely long proboscis. We found no elongation of the tip region, low numbers of proboscis sensilla, short sensilla styloconica, and no increase of galeal musculature in relation to galeal volume, but a larger food canal, as well as larger head musculature in relation to the head capsule. The results indicate the relatively low extra expense on the proboscis musculature and sensilla equipment but significant anatomical costs, such as reinforced haemolymph and suction pump musculature, as well as thick cuticular proboscis walls, which are functionally related to feeding performance in species possessing an extremely long proboscis.
Phylogenetic comparative methods are increasingly used to give new insights into the dynamics of trait evolution in deep time. For continuous traits the core of these methods is a suite of models that attempt to capture evolutionary patterns by extending the Brownian constant variance model. However, the properties of these models are often poorly understood, which can lead to the misinterpretation of results. Here we focus on one of these models - the Ornstein Uhlenbeck (OU) model. We show that the OU model is frequently incorrectly favoured over simpler models when using Likelihood ratio tests, and that many studies fitting this model use datasets that are small and prone to this problem. We also show that very small amounts of error in datasets can have profound effects on the inferences derived from OU models. Our results suggest that simulating fitted models and comparing with empirical results is critical when fitting OU and other extensions of the Brownian model. We conclude by making recommendations for best practice in fitting OU models in phylogenetic comparative analyses, and for interpreting the parameters of the OU model.
The Northern Rocky Mountain ecosystem supports rich biological diversity with many endemic and rare species. Extant endemics display two biogeographic patterns: widespread species with fragmented populations, and narrow-range endemics. These distributions are shown by the congeneric snails Anguispira kochi occidentalis and Anguispira nimapuna. These two taxa are disjunct from the remaining species of the genus, which achieves its greatest diversity in eastern North America. Given the disjunct nature of A. k. occidentalis and A. nimapuna, we here present a mtDNA phylogeny of the genus that includes both eastern and western species to assess the phylogenetic position of A. k. occidentalis and A. nimapuna. We then reconstruct the demographic history of A. k. occidentalis and A. nimapuna by analysing current patterns of genetic variation and interpreting the results considering the historical biogeography of the region. Both A. k. occidentalis and A. nimapuna represent unique taxa that are genetically and geographically distinct from their congeners. The current distribution and genetic structure of A. k. occidentalis has been shaped by both historical isolation in refugia and more recent northward shifts, whereas A. nimapuna is represented by two populations with shallow divergence in an area of long-term habitat stability.
Heterosis, Haldane and Bateson-Dobzhansky-Muller effects have been widely documented amongst a range of plants and animals. However, typically these effects are shown by taking parents of known genotype into the laboratory and measuring components of the F1 progeny under laboratory conditions. This leaves in doubt the real significance of such effects in the field. Here we use the well-known colour pattern genotypes of the African monarch or queen (Danaus chrysippus), which also control wing length, to test these effects both in the laboratory and in a contact zone in the field. By measuring the wing lengths in animals of known colour pattern genotype we show clear evidence for all three hybrid effects at the A and BC colour patterning loci, and importantly, that these same effects persist in the same presumptive F1s when measured in hybrid populations in the field. This demonstrates the power of a system in which genotypes can be directly inferred in the field and highlights that all three hybrid effects can be seen in the East African contact zone of this fascinating butterfly.
Variation in lifespan may be linked to geographic factors. While latitudinal variation in lifespan has been studied for a number of species, altitude variation has received much less attention, particularly in insects. We measured the lifespan of different populations of the Natal fruit fly Ceratitis rosa along an altitudinal cline. For the different populations we first measured the residual longevity of wild flies by captive cohort approach and compared F(1) generation from the same populations. We showed an increase in lifespan with higher altitude for a part of our data. For the field collected flies (F0) the average remaining lifespan increased monotonically with altitude for males but not for females. For the F(1) generation, longevity of both males and females of the highest-altitude population was longer than for the two other lower-altitude populations. This relationship between altitude and lifespan may be explained by the effects of temperature on reproduction. Reproductive schedules in insects are linked to temperature: lower temperature, characteristic of high-altitude sites, generally slows down reproduction. Because of a strong trade-off between reproduction and longevity, we therefore observed a longer lifespan for the high- altitude populations. Other hypotheses such as different predation rates in the different sites are also discussed.
Biogeography can illuminate spatial patterns of intraspecific morphological variation along environmental gradients. We evaluated whether body size in the common vampire bat (Desmodus rotundus) varies with climate and elevation across Colombia using 1076 museum and field specimens (1921-2023). Field specimens originated from diverse environmental conditions, including sites with mean annual temperatures ranging from 8.94 to 28.94 °C, annual precipitations from 515 to 7132 mm, and elevations from 4.6 to 3476 m a.s.l. Forearm length, a proxy for body size, was analysed with regression models, including Colombian department as a random effect. Linear models showed that forearm length decreased with mean annual temperature (females: R 2 = .023, β = -.143, P = .006; males: R 2 = .044, β = -.173, P = 1.03 × 10-5) and increased with elevation (females: R 2 = .038, β = .001, P = 3.66 × 10-4; males: R 2 = .039, β = .001, P = 3.35 × 10-5), with an overall decrease of .19 mm per 1°C across all individuals. In contrast, linear mixed-effects models found no significant effects of temperature, elevation, precipitation, or latitude. These contrasting results suggest data limitations and that patterns detected by simpler models disappear when accounting for the spatial structure of the sampling. We argue that temperature is not a robust predictor of body size in D. rotundus. Our findings advance the biogeography of D. rotundus and provide a foundation for the uncertainty of climate change effects on bat morphology.
Life-history characteristics of female threespine stickleback (Gasterosteus aculeatus) were examined in 12 populations, 11 freshwater and one anadromous, within the Cook Inlet region of Alaska. Because this area has been deglaciated during the last 20 000 years, the freshwater populations are recently derived, probably independently, from the local marine or anadromous stickleback. Freshwater threespine stickleback have undergone considerable morphological evolution within this region, apparently in response to environmental factors including predatory regimes and environmental productivity. Our freshwater study populations were selected to sample this range of morphological variation in order to determine whether life-history traits and morphologies have followed similar evolutionary trajectories. Freshwater populations could be categorized generally into one of three ecomorphotypes: those inhabiting relatively productive lakes having one or more piscivorous fishes present, and in which the stickleback exhibit a fully developed pelvic girdle; those inhabiting low-calcium lakes that lack piscivorous fishes, and in which the pelvic structures are incomplete; those living in streams with piscivorous fishes, in which the stickleback have fully developed pelvic girdles. The anadromous population constituted a fourth ecomorphotype that lives in marine waters, and is robustly armored. The freshwater populations showed considerable variation in all life-history traits assessed, and this variation generally corresponded to our ecomorphological classifications. Nevertheless, within each ecomorphotype there was sufficient variation to suggest that morphological and life-history traits may not always respond in the same manner in response to the same selective regime.Copyright 1998 The Linnean Society of London