Masquerade is associated with polyphagy and larval overwintering in Lepidoptera

Masquerading animals benefit from the difficulty that predators have in differentiating them from the inedible objects, such as twigs, that they resemble. The function of masquerade has been demonstrated, but how it interacts with the life history of organisms has not yet been studied. Here, we report the use of comparative analyses to test hypotheses linking masquerade to life‐history parameters. We constructed a phylogenetic tree of the British species of the lepidoptera families Geometridae and Drepanidae, and compiled life history and coloration data from the literature. We found that masquerade is associated with the exploitation of a greater diversity of host plants whether measured by the number of families or genera. We found a positive relationship between body size and polyphagy among masquerading species, and no relationship among cryptic species. Among those species predominantly found on woody host plants, masquerading species are more likely to overwinter as larvae while cryptic species mostly overwinter as pupae. Polyphenism was associated with multivoltinism in masquerading species but not cryptic species. Taken together, our results show that masquerade must be viewed as a strategy distinct to crypsis and hence may provide insights into the evolution of both defensive strategies. Our study further demonstrates the utility of broad‐scale between‐species comparisons in studying associations between diverse life‐history parameters and sensory aspects of predator‐prey interactions. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 90–103.     

Defensive masquerade by plants

The defensive strategy known as masquerade, or camouflage without crypsis (a type of deception that partly overlaps mimicry) has received little scientific attention in animals, and concerning plants even less. Moreover, when cases of masquerade were described in plants, they were considered as camouflage or other types of defence through mimicry. Masquerade (including in plants) may operate not only through vision, but also via other senses. Here I review several types of published cases of masquerade in plants, although they were not defined as such when published, and propose that there are two different types of masquerade in plants: (1) non‐plant‐mimicking defensive masquerade, in which they look (or smell) like uninteresting objects to herbivores (look like a stone or an animal, or smell like droppings or carrion, etc.), and (2) plant‐mimicking defensive masquerade, in which plants or plant parts do not look appealing for herbivores, not being green, looking dead or old, harbouring insects, already attacked, less nutritious, etc. Defensive masquerade by plants may in many cases be non‐exclusive, but serve additional physiological and defensive functions or operate simultaneously with other defences. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 1162–1166.     

The evolution of placentas and superfetation in the fish genus Poecilia (Cyprinodontiformes: Poeciliidae: subgenera Micropoecilia and Acanthophacelus)

Complex adaptations are often found in nature, although our ability to discern how and why such traits evolved is limited because their origin occurred in the distant past and the details of their evolution have been lost through extinction (e.g. all placental mammals inherited their placentas from a single common ancestor that lived over 100 Mya). In poeciliid fishes, placentas have evolved independently multiple times and portions of the path to the evolution of complexity can be found in living species. In the present study, we describe the life histories of six species within the genus Poecilia that includes the subgenera Micropoecilia and Acanthophacelus (the guppy; Poecilia reticulata). We demonstrate that extensive placentotrophy and superfetation, the ability to simultaneously carry more than one developing brood, have evolved within this clade. These fish represent the third clade in which we have discovered the independent origin of a placenta that also includes close relatives that lack a placenta. We discuss possible adaptive advantages of the joint evolution of extensive placentation and superfetation in these fishes. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 784–796.     

Patterns of ecomorphological convergence among mainland and island Anolis lizards

Differing selective pressures on islands versus the mainland may produce alternative evolutionary outcomes among closely related lineages. Conversely, lineages may be constrained to produce similar outcomes in different mainland and island environments, or mainland and island environments may not differ significantly. Among the best‐studied island radiations are Caribbean Anolis lizards. Distinct morphotypes, or ‘ecomorphs’, have been described, and the same ecomorphs have evolved independently on each Greater Antillean island. The mainland Anolis radiation has received much less attention. We use a large morphological data set and a novel phylogenetic hypothesis to show that mainland Anolis did not evolve the same morphotypes as island Anolis, despite some island species being more closely related to mainland species than to island species that share their morphotype. A maximum of four of the six Caribbean ecomorphs were found to exist on the mainland, and just 15 of 123 mainland species are assignable to a Caribbean ecomorph. This result was insensitive to differing taxon samples and alternative phylogenetic hypotheses. Mainland convergence to a Caribbean ecomorph occurs only among species assigned to the grass‐bush ecomorph. Thus, the ecomorphs that have evolved convergently multiple times in the Caribbean have not evolved in parallel on the mainland. These results are consistent with the hypothesis that mainland and island environments offer different selective pressures. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 852–859.     

The distribution of circularly polarized light reflection in the Scarabaeoidea (Coleoptera)

The light reflected from many scarab beetles is strongly circularly polarized, a phenomenon that may be unique in nature. Approximately 1500 genera and more than 19 000 species/subspecies of scarab beetles (Scarabaeoidea) in the collection of the Natural History Museum, London, were surveyed with circularly polarizing filters to assess how widespread this effect is and how it relates to colour patterns in the individuals concerned. Over 1100 measurements were made of the strength of the circular polarization, in some cases registering 97%. Circular polarization had been previously described from five subfamilies of Scarabaeidae and, in the present study, was found in three further subfamilies: Phaenomeridinae, Dynastinae and Euchirinae, as well as in the subfamily Ceratocanthinae of the family Hybosoridae, comprising the first records outside the Scarabaeidae. The results may have implications for the taxonomy of the group, for visual discrimination, and for the behaviour of the species themselves. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 585–596.     

The origin of mammalian endothermy: a paradigm for the evolution of complex biological structure

Several mutually incompatible theories exist about how and why endothermy evolved in mammals and birds. Some take the primary function to have been thermoregulation, selected for one adaptive purpose or another. Others take the high aerobic metabolic rate to have been primary. None of these theories is incontrovertibly supported by evidence, either from the fossil record of the synapsid amniotes or from observations and experiments on modern organisms. Furthermore, all are underpinned by the tacit assumption that endothermy must have evolved in a stepwise pattern, with an initial adaptive function followed only later by the addition of further functions. It is argued that this assumption is unrealistic and that the evolution of endothermy can be explained by the correlated progression model. Each structure and function associated with endothermy evolved a small increment at a time, in loose linkage with all the others evolving similarly. The result is that the sequence of organisms maintained functional integration throughout, and no one of the functions of endothermy was ever paramount over the others. The correlated progression model is tested by the nature of the integration between the parts as seen in living mammals, by computer simulations of the evolution of complex, multifunctional, multifactorial biological systems, and by reference to the synapsid fossil record, which is fully compatible with the model. There are several potentially important implications to be drawn from this example concerning the study of the evolution of complex structure and the new higher taxa that manifest it.  © 2006 The Linnean Society of London, Zoological Journal of the Linnean Society , 2006, 147 , 473–488.     

Parallel evolution of termite‐egg mimicry by sclerotium‐forming fungi in distant termite groups

Among the great diversity of insect–fungus associations, fungal mimicry of termite eggs is a particularly fascinating consequence of evolution. Along with their eggs, Reticulitermes termites often harbour sclerotia of the fungus Fibularhizoctonia sp., called ‘termite balls’, giving the fungus competitor‐free habitat within termite nests. The fungus has evolved sophisticated morphological and chemical camouflage to mimic termite eggs. To date, this striking insect–fungus association has been found in eight temperate termite species, but is restricted to the lower termite genera Reticulitermes and Coptotermes. Here, we report the discovery of a novel type of termite ball (‘Z‐type’) in the subtropical termite, Nasutitermes takasagoensis. Phylogenetic analysis indicated that the Z‐type termite ball is an undescribed Trechisporoid fungus, Trechispora sp., that is phylogenetically distant from Fibularhizoctonia, indicating two independent origins of termite‐egg mimicry in sclerotium‐forming fungi. Egg protection bioassays using dummy eggs revealed that Reticulitermes speratus and N. takasagoensis differ in egg‐size preference. A comparative study of termite ball size and egg‐size preference of host termites showed that both fungi evolved a termite ball size that optimized the acceptance of termite balls as a unit investment. Termite‐egg mimicry by these fungi offers a model case of parallel evolution. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 531–537.     

Thermal effects on reptile reproduction: adaptation and phenotypic plasticity in a montane lizard

Interspecific comparisons suggest a strong association between cool climates and viviparity in reptiles. However, intraspecific comparisons, which provide an opportunity to identify causal pathways and to distinguish facultative (phenotypically plastic) effects from canalized (genetically fixed) responses, are lacking. We documented the reproductive traits in an alpine oviparous lizard, and manipulated thermal regimes of gravid females and their eggs to identify proximate causes of life‐history variation. Embryonic development at oviposition was more advanced in eggs laid by females from high‐elevation populations than in eggs produced by females from lower elevations. In the laboratory, experimentally imposed low maternal body temperatures delayed oviposition and resulted in more advanced embryonic development at oviposition. Warm conditions both in utero and in the nest increased hatching success and offspring body size. Our intraspecific comparisons support the hypothesis that viviparity has evolved in cold‐climate squamates because of the direct fitness advantages that warm temperatures provide developing offspring. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 642–655.     

Explaining patterns in modern ruminant diversity: contingency or constraint?

Bovid species outnumber those of cervids by over two and half to one. The present study attempts to explain this difference using two principle concepts: contingency and constraint. The concept of contingency considers the role of biogeography and the distributions and timings of major dispersals seen in the two families. Although this historical context is considered vital for understanding the problem, cervids are also characterized by their global absence from open and arid grassland habitats. This is explained in terms of phylogenetic constraint. One proposal considers the deciduous antlers of cervids as constraining the group to higher quality forage that is not generally associated with open habitats. Alternatively and more generally applicable to all ruminants is the ‘cusp fusion hypothesis’, presented here for the first time. The hypothesis seeks to explain how the primitive ruminant molar state, as seen in modern cervids and giraffids, prevents the attainment of very high molar crowns and, with it, the ability to cope with high rates of dietary tooth wear. Conversely, the derived condition of precocial cusp fusion seen in the Bovidae and Antilocapridae has enabled higher tooth crowns, their expansion into open habitats, and an increased diversity potential. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 657–672.     

Structure and function of defensive glands in soldiers of Glossotermes oculatus (Isoptera: Serritermitidae)

The soldier caste represents the most conspicuous realization of termite eusociality, characterized by an extreme anatomical, behavioural, and physiological specialization. Numerous strategies have evolved in soldiers, including extreme adaptations such as self‐sacrifice by autothysis. In the present study, we investigated the structure and function of defensive glands in Glossotermes oculatus soldiers aiming to understand their use in combat. Three glands are involved in defence: labral, frontal, and labial glands. Mandibles are used to bite the enemy, whereas the secretions of labral and labial glands are discharged into the wound. A striking characteristic of G. oculatus is the lack of the frontal pore; the secretion of the frontal gland is discharged by a rupture of the body wall. We hypothesized that this self‐sacrifice is an efficient way of blocking a gallery under attack. A similar development of the frontal gland occurs in Serritermes serrifer, which supports the close relationship between the two genera inferred from morphological and genetic analyses. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 839–848.     

Do constructional constraints influence cyprinid (Cyprinidae: Leuciscinae) craniofacial coevolution?

Constraints on form may determine how organisms diversify. As a result of competition for the limited space within the body, investment in adjacent structures could represent an evolutionary compromise. For example, evolutionary trade‐offs resulting from limited space in the head could have influenced how the sizes of the jaw muscle, as well as the eyes, evolved in North American cyprinid fishes. To test the evolutionary independence of the size of these structures, we measured the mass of the three major adductor mandibulae muscles and determined the eye volume in 36 cyprinid species. Using a novel phylogeny, we tested the hypotheses that the sizes of these four structures were negatively correlated with each other during cyprinid evolution. We found that evolutionary change in the adductor mandibulae muscles was generally positively and/or not correlated, suggesting that competition for space among cyprinid jaw muscles has not influenced their evolution. However, there was a negative relationship between mass of adductor mandibulae 1 and eye volume, indicating that change in these physically adjacent structures is consistent with an evolutionary constructional constraint. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 136–146.     

Inbreeding depression in the effects of body mass on energy use

Large organisms have higher metabolic rates than small organisms but, if we compare their relative metabolic rates (i.e. per gram of tissue), this relationship is very often reversed. The pervasiveness of this phenomenon, called metabolic scaling, has attracted several theoretical explanations, and also produced lingering debate over whether metabolic scaling is a physically constrained and universally constant phenomenon or a more variable and evolutionarily malleable trait. To bring novel insights to this debate, we manipulated male Gryllodes sigillatus crickets' coefficients of inbreeding to determine whether metabolic scaling is sensitive to the manipulation of genetic quality. Because inbreeding depression is inversely related to past selection, our results indicate that selection has favoured an overall lower metabolic rate and a less steep slope of metabolic scaling. Altered metabolic scaling as a result of inbreeding was found to be caused by increased variation in metabolic rate, suggesting the existence of balancing selection towards intermediate metabolic rates. Although we found effects of inbreeding on metabolic scaling, much of the relationship between body mass and metabolic rate remained unexplained, leaving plenty of room for speculation concerning the fixed constraints that might affect evolutionary trajectories. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 309–317.     

Litter‐trapping plants: filter‐feeders of the plant kingdom

Litter‐trapping plants have specialized growth habits and morphologies that enable them to capture falling leaf litter and other debris, which the plants use for nutrition after the litter has decayed. Litter is trapped via rosettes of leaves, specially modified leaves and/or upward‐growing roots (so‐called ‘root baskets’). Litter‐trappers, both epiphytic and terrestrial, are found throughout the tropics, with only a few extra‐tropical species, and they have evolved in many plant families. The trapped litter mass is a source of nutrients for litter‐trapping plants, as well as food and housing for commensal organisms. Despite their unique mode of life, litter‐trapping plants are not well documented, and many questions remain about their distribution, physiology and evolution.–© 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 179 , 554–586.     

Multilocus phylogeography of the flightless darkling beetle Nyctoporis carinata (Coleoptera: Tenebrionidae) in the California Floristic Province: deciphering an evolutionary mosaic

The California Floristic Province (CFP) is considered a global biodiversity hotspot because of its confluence of high species diversity across a wide range of threatened habitats. To understand how biodiversity hotspots such as the CFP maintain and generate diversity, we conducted a phylogeographic analysis of the flightless darkling beetle, Nyctoporis carinata, using multiple genetic markers. Analyses of both nuclear and mitochondrial loci revealed an east–west genetic break through the Transverse Ranges and high genetic diversity and isolation of the southern Sierra Nevada Mountains. Overall, the results obtained suggest that this species has a deep evolutionary history whose current distribution resulted from migration out of a glacial refugium in the southern Sierra Nevada via the Transverse Ranges. This finding is discussed in light of similar genetic patterns found in other taxa to develop a foundation for understanding the biodiversity patterns of this dynamic area. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 424–444.     

Climate cooling promoted the expansion and radiation of a threatened group of South American orchids (Epidendroideae: Laeliinae)

The Brazilian Cerrado is the most species‐rich tropical savanna in the world. Within this biome, the Campos Rupestres (‘rocky savannas’) constitute a poorly studied and highly threatened ecosystem. To better understand how plants characteristic of this vegetation have evolved and come to occupy the now widely‐separated patches of rocky formations in eastern Brazil, we reconstruct the biogeographical history of the rare orchid genus Hoffmannseggella. We apply parsimony and Bayesian methods to infer the phylogenetic relationships among 40 out of the 41 described species. Absolute divergence times are calculated under penalized likelihood and compared with estimates from a Bayesian relaxed clock. Ancestral ranges are inferred for all nodes of the phylogeny using Fitch optimization and statistical dispersal vicariance analysis. In all analyses, phylogenetic uncertainty is taken into account by the independent analysis of a large tree sample. The results obtained indicate that Hoffmannseggella underwent rapid radiation around the Middle/Late Miocene (approximately 11–14 Mya). The region corresponding today to southern Minas Gerais acted as a main source area for several independent range expansions north‐ and eastwards via episodic corridors. These results provide independent evidence that climate cooling following the Middle Miocene Climatic Optimum (approximately 15 Mya) led to important vegetational shifts in eastern Brazil, causing an increase in the dominance of open versus closed habitats. Polyploidy following secondary contact of previously isolated populations may have been responsible for the formation of many species, as demonstrated by the high ploidy levels reported in the genus. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 597–607.     

Morphological and molecular taxonomy of a new Daptonema (Nematoda,Xyalidae) with comments on the systematics of some related taxa

A new species of Daptonema is described based upon morphological characters and 18S rRNA sequence. Daptonema matrona sp. nov. was collected in Pina Basin (north‐eastern Brazil). It differs from all other species of the genus by the presence of reduced cephalic setae and straight spicules. These features require an adaptation of the generic diagnosis. Moreover, the females are characterized by intra‐uterine development of the offspring, considered herein as their major autapomorphic feature. Molecular systematic analyses supported Daptonema matrona sp. nov. as a distinct genetic and evolutionary lineage. The data also indicate hypotheses of taxonomic synonymies amongst some related taxa from Xyalidae as well as the paraphyly of Daptonema. © 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 158 , 1–15.     

Influence of different substrates on the evolution of morphology and life‐history traits of azooxanthellate solitary corals (Scleractinia: Flabellidae)

Sessile organisms are influenced considerably by their substrate conditions, and their adaptive strategies are key to understanding their morphologic evolution and traits of life history. The family Flabellidae (Cnidaria: Scleractinia) is composed of the representative azooxanthellate solitary corals that live on both soft and hard substrates using various adaptive strategies. We reconstructed the phylogenetic tree and ancestral character states of this family from the mitochondrial 16S and nuclear 28S ribosomal DNA sequences of ten flabellids aiming to infer the evolution of their adaptive strategies. The Javania lineage branched off first and adapted to hard substrates by using a tectura‐reinforced base. The extant free‐living flabellids, including Flabellum and Truncatoflabellum, invaded soft substrates and acquired the flabellate corallum morphology of their common ancestor, followed by a remarkable radiation with the exploitation of adaptive strategies, such as external soft tissue [e.g. Flabellum (Ulocyathus)], thecal edge spine, and transverse division (e.g. Placotrochus and Truncatoflabellum). Subsequently, the free‐living ancestors of two genera (Rhizotrochus and Monomyces) invaded hard substrates independently by exploiting distinct attachment apparatuses such as tube‐like and massive rootlets, respectively. In conclusion, flabellids developed various morphology and life‐history traits according to the differences in substrate conditions during the course of their evolution. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 184–192.     

Evolution of ontogenetic allometry shaping giant species: a case study from the damselfish genus Dascyllus (Pomacentridae)

The evolution of body size, the paired phenomena of giantism and dwarfism, has long been studied by biologists and paleontologists. However, detailed investigations devoted to the study of the evolution of ontogenetic patterns shaping giant species are scarce. The damselfishes of the genus Dascyllus appear as an excellent model for such a study. Their well understood phylogeny reveals that large‐bodied species have evolved in two different clades. Geometric morphometric methods were used to compare the ontogenetic trajectories of the neurocranium and the mandible in both small‐bodied (Dascyllus aruanus and Dascyllus carneus; maximum size: 50–65 mm standard length) and giant (Dascyllus trimaculatus and Dascyllus flavicaudus; maximum size: 90–110 mm standard length) Dascyllus species. At their respective maximum body size, the neurocranium of the giant species is significantly shorter and have a higher supraoccipital crest relative to the small‐bodied species, whereas mandible shape variation is more limited and is not related to the ‘giant’ trait. The hypothesis of ontogenetic scaling whereby the giant species evolved by extending the allometric trajectory of the small‐bodied ones (i.e. hypermorphosis) is rejected. Instead, the allometric trajectories vary among species by lateral transpositions. The rate of shape changes and the type of lateral transposition also differ according to the skeletal unit among Dascyllus species. Differences seen between the two giant species in the present study demonstrate that giant species may appear by varied alterations of the ancestor allometric pattern. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 99–117.     

Predators are less likely to misclassify masquerading prey when their models are present

Masquerading animals have evolved striking visual resemblances to inanimate objects. These animals gain protection from their predators not simply by avoiding detection, but by causing their predators to misclassify them as the ‘models’ that they appear to resemble. Using domestic chicks as predators and twig-mimicking caterpillars as prey, we demonstrated that masquerading prey were more likely to be misclassified as their models when viewed in isolation from their models than when viewed alongside examples of their model, although they benefitted from masquerade to some extent in both conditions. From this, we predict a selection pressure on masqueraders to use microhabitats that reduce the risk of them being viewed simultaneously with examples of their model, and/or to more closely resemble their model in situations where simultaneous viewing is commonplace.     

How to become a yucca moth: minimal trait evolution needed to establish the obligate pollination mutualism

The origins of obligate pollination mutualisms, such as the classic yucca–yucca moth association, appear to require extensive trait evolution and specialization. To understand the extent to which traits truly evolved as part of establishing the mutualistic relationship, rather than being pre‐adaptations, we used an expanded phylogenetic estimate with improved sampling of deeply‐diverged groups to perform the first formal reconstruction of trait evolution in pollinating yucca moths and their nonpollinating relatives. Our analysis demonstrates that key life‐history traits of yucca moths, including larval feeding in the floral ovary and the associated specialized cutting ovipositor, as well as colonization of woody monocots in xeric habitats, may have been established before the obligate mutualism with yuccas. Given these pre‐existing traits, novel traits in the mutualist moths are limited to the active pollination behaviours and the tentacular appendages that facilitate pollen collection and deposition. These results suggest that a highly specialized obligate mutualism was built on the foundation of pre‐existing interactions between early Prodoxidae and their host plants, and arose with minimal trait evolution. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 847–855.