Life cycle polyphenism as a factor affecting ecological divergence within <Emphasis Type="Italic">Notophthalmus viridescens</Emphasis>

Polyphenism, which allows a single genotype to express multiple discrete phenotypes in response to environmental cues, is an adaptive trait in heterogeneous environments. Pond hydroperiod is an important ecological parameter affecting amphibian life history, and variation in local pond hydrology has been hypothesized to play a role in species divergence via changes in polyphenism. The eastern newt (Notophthalmus viridescens) expresses life cycle polyphenism. Larvae develop along three possible pathways: metamorphosis to aquatic lunged adult via a terrestrial juvenile (eft) stage, metamorphosis directly to an aquatic lunged adult, or maturation directly to an aquatic gilled adult without metamorphosis (i.e., paedomorphosis). Subspecies of N. viridescens vary in their polyphenic patterns, suggesting possible adaptation to different environments. However, no studies have experimentally tested how genetic and environmental components contribute to the observed differences among subspecies and whether such differences may facilitate divergence. We tested whether adaptation to local pond hydrology via polyphenic changes existed among subspecies by rearing larvae of three subspecies (N. v. dorsalis, N. v. louisianensis, and N. v. viridescens) along three hydroperiod regimes (short, long, and constant) in outdoor artificial ponds. We found that larval N. v. viridescens obligately metamorphosed to efts under all hydroperiods, whereas N. v. dorsalis and N. v. louisianensis exhibited plasticity: larvae metamorphosed to efts under drying conditions but metamorphosed directly to aquatic adults or became paedomorphic in constant water. Also, N. v. viridescens metamorphosed to efts faster and at a smaller body size than the other two subspecies. These data suggest that subspecies of N. viridescens are adapted to different pond hydroperiods, supporting the potential for polyphenism to facilitate divergence. Canalizing selection for certain alternative phenotypes within a single species in which other populations remain plastic may play an important role in the initiation of ecological divergence.     

On the role of sexual selection in ecological divergence: a test of body‐size assortative mating in the eastern newt Notophthalmus viridescens

Speciation processes initiated by divergent selection often fail to complete; yet, how sexual selection is involved in the progress of ecological speciation is rarely understood. Intraspecific body‐size variation affects mate preference and male–male competition, which can consequently lead to assortative mating based on body size. In the present study, we tested the importance of body size difference in the potential of assortative mating between the two eastern newt subspecies, larger Notophthalmus viridescens viridescens and smaller Notophthalmus viridescens dorsalis. Through differential expression of life‐cycle polyphenism, these two subspecies are adapted to contrasting environments, which has likely led to the subspecific body‐size difference. We found that males of both subspecies preferred larger females of N. v. viridescens as mates presumably because of the fecundity advantage of larger females. On the other hand, no evidence of female choice was found. Larger males of N. v. viridescens exhibited greater competitive ability and gained primary access to larger females of their own kind. However, smaller males were able to overcome their inferior competitive ability by interfering with larger males' spermatophore transfer and sneakily mating with larger females. Thus, the subspecific body‐size difference importantly affected sexual selection processes, resulting in nonrandom but not completely assortative mating patterns between the larger and smaller subspecies. Although life‐cycle polyphenism facilitates the intraspecific ecological divergence within N. v. viridescens sexual selection processes, namely smaller males' mate preference for larger females and sexual interference during spermatophore transfer, may be halting completion of the ecological speciation. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 884–897.     

Will pre‐adaptation buffer the impacts of climate change on novel species interactions?

Species are expected to alter their ranges as climates change. Climate‐induced range expansions of predators could threaten evolutionarily naïve prey populations, leading to high mortality at the invasion front. If prey can apply existing defenses against local predators to novel predation threats induced by climate change, mortality threats will be less than expected. Here, we examine if spotted salamander larvae Ambystoma maculatum from populations that coexist with native red‐spotted newts Notophthalmus viridescens survive better when exposed to a novel predator, the marbled salamander Ambystoma opacum. We show that regional mean winter temperatures warmed 2.0°C over 116 yr in the region, and that A. opacum survival increases in ponds with higher winter temperatures. Hence as winters continue to warm, this apex predator will likely colonize ponds north of their current range limit. Next, we performed common garden experiments to determine if local adaptations to native N. viridescens and exposure to A. opacum or N. viridescens kairomones (predator chemical cues) altered A. maculatum survival in predation trials. We did not find evidence for local adaptation to N. viridescens. However, A. maculatum from high‐N. viridescens ponds that were reared with A. opacum kairomones suffered significantly higher mortality from the native predator N. viridescens. This outcome suggests an unanticipated interaction between local adaptation and plastic responses to novel kairomones from a potentially range‐expanding predator. Current projections of biodiversity losses from climate change generally ignore the potential for eco‐evolutionary interactions between native and range‐expanding species and thus could be inaccurate.     

Chytridiomycosis impacts predator-prey interactions in larval amphibian communities

Despite ecologists increasingly recognizing pathogens as playing significant roles in community dynamics, few experimental studies have quantified patterns of disease impacts on natural systems. Amphibians are experiencing population declines, and a fungal pathogen (Batrachochytrium dendrobatidis; Chytridiomycota) is a suspected causal agent in many declines. We studied the effects of a pathogenic fungus on community interactions between the gray treefrog, Hyla chrysoscelis, and eastern newts, Notophthalmus viridescens. Recent studies have characterized chytridiomycosis as an emerging infectious disease, whose suspected rapid range expansion and widespread occurrence pose a significant risk for amphibian populations worldwide. We reared larvae in outdoor polyethylene experimental tanks and tested the effects of initial larval density, predator presence, and fungal exposure on Hyla recruitment and predator-prey interactions between Hyla and Notophthalmus. Newts reduced treefrog survival, and high intraspecific density decreased metamorphic body mass independent of B. dendrobatidis. The presence of fungi reduced treefrog body mass at metamorphosis by 34%, but had no significant main effect on survival or larval period length. B. dendrobatidis differentially affected larval development in the presence of predators; Hyla developed slower when reared with the pathogen, but only when newts were present. This significant predator-by-pathogen interaction suggests that the impact of chytridiomycosis on larval amphibians may be exacerbated in complex communities. Our data suggest that B. dendrobatidis effects on host life history may be complex and indirect. Direct measurements of the community-level effects of pathogens offer an important opportunity to understand a significant threat to global biodiversity—declining amphibian populations.     

Photoperiod,stress and the distribution of leukocytes in the peripheral blood ofNotophthalmus viridescens

Summary Adult newts,Notophthalmus viridescens, were maintained for 8 days at a constant temperature of 11.0±0.5 °C. In one series, the control animals were kept in constant darkness (DD), while the experimental newts were exposed to alternating 12-hour periods of light and dark (LD). In a second series, controlNotophthalmus lived in DD, and experimental animals lived in constant light (LL). In both series, the newts were sacrificed on the ninth day when blood smears were prepared. Differential counts of the leukocytes of animals that lived under the LD regimen were the same as those of controlNotophthalmus (Table 1). However, in newts that were maintained in LL, the neutrophils increased and the lymphocytes decreased relative to those types of cells in the controls (Table 1). Those changes indicate that continuous light constitutes stress for this species.Supported in part by a grant from the Committee on Research, Travel and Sabbatical Leaves, Colby College     

Genetic comparison of wild populations ofLepilemur septentrionalis andLepilemur dorsalis using RAPD markers

The genetic polymorphism of Malagasy prosimian populations is studied by using RAPD markers. The analysis includes twoLepilemur septentrionalis populations of the area of Analamera separated by a deforested hill crest and one population ofL. dorsalis from the island of Nosy-Be. The genetic diversity is higher in the two populations of Analamera than in that of Nosy-Be and the level of genetic differentiation is higher between the population ofL. dorsalis and the two populations ofL. septentrionalis than between the two populations ofL. septentrionalis themselves. Despite the hill crest separating the two populations ofL. septentrionalis, our results demonstrate that they belong to one population. The respective roles of the geographical barriers and the reproductive barrier between the two species, are discussed.     

Predator size and phenology shape prey survival in temporary ponds

Theoretical efforts suggest that the relative sizes of predators and their prey can shape community dynamics, the structure of food webs, and the evolution of life histories. However, much of this work has assumed static predator and prey body sizes. The timing of recruitment and the growth patterns of both predator and prey have the potential to modify the strength of predator–prey interactions. In this study, I examined how predator size dynamics in 40 temporary ponds over a 3-year period affected the survival of spotted salamander (Ambystoma maculatum) larvae. Across communities, gape-limited predator richness, but not size, was correlated with habitat duration (pond permanence). Within communities, mean gape-limited predator size diminished as the growing season progressed. This size reduction occurred because prey individuals grew into a body size refuge and because the largest of the predators left ponds by mid-season. Elevated gape-limited predation risk across time and space was predicted by the occurrence of two large predatory salamanders: marbled salamander larvae (Ambystoma opacum) and red-spotted newt adults (Notophthalmus viridescens). The presence of the largest gape-limited predator, A. opacum, predicted A. maculatum larval survival in the field. The distribution of large predatory salamanders among ponds and across time is expected to lead to differing community dynamics and to generate divergent natural selection on early growth and body size in A. maculatum. In general, a dynamic perspective on predator size often will be necessary to understand the ecology and evolution of species interactions. This will be especially true in frequently disturbed or seasonal habitats where phenology and ontogeny interact to determine body size asymmetries. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Model toxin level does not directly influence the evolution of mimicry in the salamander <Emphasis Type="Italic">Plethodon cinereus</Emphasis>

The resemblance between palatable mimics and unpalatable models in Batesian mimicry systems is tempered by many factors, including the toxicity of the model species. Model toxicity is thought to influence both the occurrence of mimicry and the evolution of mimetic phenotypes, such that mimicry is most likely to persist when models are particularly toxic. Additionally, model toxicity may influence the evolution of mimetic phenotype by allowing inaccurate mimicry to evolve through a mechanism termed ‘relaxed selection’. We tested these hypotheses in a salamander mimicry system between the model Notophthalmus viridescens and the mimic Plethodon cinereus, in which N. viridescens toxicity takes the form of tetrodotoxin. Surprisingly, though we discovered geographic variation in model toxin level, we found no support for the hypotheses that model toxicity directly influences either the occurrence of mimicry or the evolution of mimic phenotype. Instead, a link between N. viridescens size and toxicity may indirectly lead to relaxed selection in this mimicry system. Additionally, limitations of predator perception or variation in the rate of phenotypic evolution of models and mimics may account for the evolution of imperfect mimicry in this salamander species. Finally, variation in predator communities among localities or modern changes in environmental conditions may contribute to the patchy occurrence of mimicry in P. cinereus.     

Patterns of genetic differentiation in two annual bromegrasses,Bromus lanceolatus andB. hordeaceus (Poaceae)

Infraspecific genetic differentiation was analysed in two tetraploid annual bromegrasses,Bromus lanceolatus (from N Africa) andB. hordeaceus (from N Africa and France). Genetic analysis of populations was based on allozyme polymorphisms at 17 loci. Different fixed heterozygous phenotypes were scored in both species, according to their allopolyploid origin. In N Africa, more variation occurred among populations ofB. lanceolatus than ofB. hordeaceus. The variation was not randomly distributed among populations of both species. InB. lanceolatus, differentiation was correlated with climatic variables rather than with geographic distance between populations. Higher correlation of genetic differentiation with geographic distance occurred inB. hordeaceus, particularly at large geographic scale, between French and N African populations. Within each region, the populations appeared weakly genetically differentiated, even when belonging to different subspecies.     

Trinitrobenzene sulfonic acid effects in two amphibian model systems

The induction of hapten-specific tolerance was investigated in two amphibia, Notophthalmus viridescens and Xenopus laevis. Responses to trinitrophenylated (TNP)-Ficoll and TNP-lipopolysaccharide (LPS), as well as to horse erythrocytes (HRBC) were examined in both species, following an intraperitoneal injection of 2,4,6-trinitrobenzenesulfonic acid (TNBS). The less evolutionarily advanced newt, Notophthalmus, failed to respond to all three immunogens after TNBS administration. While Xenopus became completely tolerant upon challenge with TNP-Ficoll and partially tolerant with TNP-LPS, full capacity to respond to HRBC was retained. Therefore, specific tolerance was induced in Xenopus, but not in Notophthalmus. The tolerance with TNP-Ficoll in the toad, Xenopus, was short lived and return to responsiveness appeared to be related inversely to levels of TNP protein in the sera of TNBS-treated animals. The thymic dependence of this tolerance could not be determined, because adult thymectomy (ATx) abrogated the response to TNP-Ficoll in control nontolerized animals. Responses to TNP-LPS and HRBC were unaffected by ATx. These data, in conjunction with TNBS-induced differential tolerance to the TNP moiety, suggest carrier-dependent hapten-specific B-cell heterogeneity in the toad which differs in certain ways from that recently described for murine systems.     

Conservation genetics of the central newt (Notophthalmus viridescens) in Iowa: the importance of a biogeographic framework

In light of global declines in amphibian populations, genetic data have become increasingly important for understanding population structure and for revealing hidden diversity. At the species level, Notophthalmus viridescens is an IUCN species of “least concern”, but the subspecies N. v. louisianensis (central newt) is listed as “threatened” in Iowa, a state on the western periphery of the species range. Genetic data were collected from 282 N. v. louisianensis from 14 sites in Iowa. Sequences from 1,054 nucleotides of mitochondrial DNA from Iowa newts revealed unexpected diversity in the form of two major haplotype groups that are not sister clades, with southern Iowa N. v. louisianensis being more closely related to N. v. piaropicola (peninsula newt) from Florida than to consubspecifics in Iowa. Sequence differentiation indicates that the two lineages of newts present in Iowa diverged near the beginning of the Pleistocene. Northern and southern Iowa haplotypes were found together at one site, indicating an opportunity for hybridization near Remington’s biogeographic suture zone 1, a hotspot for hybridization in other species. Three microsatellite loci provided additional evidence for distinctness of northern and southern Iowa newt populations. This study highlights the relevance of historical biogeography to conservation, as management strategies for N. v. louisianensis in Iowa must reflect previously unrecognized diversity in this species. Nuclear and mitochondrial data indicate genetic isolation of nearby populations on the same drainage, and field data suggest the decline of one study population, emphasizing the need for identification and protection of newt breeding sites in Iowa.     

Preliminary analysis of numerical taxonomy of the genusSaguinus based on dental measurements

Although several investigations have been made from different viewpoints, the classification or interspecific relationships ofSaguinus still remain uncertain. In the present study, we applied multivariate analysis methods to dental measurements of part ofSaguinus populations of sufficient sample size and obtained the following conclusions.Saguinus can be classified into two main groups: one consists ofS. oedipus andS. leucopus, and the other ofS. fuscicollis, S. nigricollis, S. labiatus, andS. mystax. Concerning the former group, the two subspecies ofS. oedipus, S. o. oedipus, andS. o. geoffroyi, show a close affinity with each other and also a close relationship toS. leucopus, while the latter group consists of two subgroups of species, one includingS. fuscicollis andS. nigricollis, and the other includingS. labiatus andS. mystax. The biological distance betweenS. oedipus oedipus andS. o. geoffroyi is slightly larger than that between the pairs ofS. fuscicollis andS. nigricollis and ofS. labiatus andS. mystax. Factor analysis revealed significant factors which could explain the differences among the seven maleSaguinus populations. Taking all the results into account, it seems necessary to reconsider the phylogenetic relationships within the genusSaguinus.     

Notes on the geographic distribution of howling monkeys in the marajó archipelago, pará, Brazil

I review the distribution of genus Alouattain the Marajó Archipelago based on geographic variation of pelage color patterns. Specific differences exist among the labeled specimens at Museu Paraense Emílio Goeldi, which are confirmed via new field information from wild populations. The animals from Marajó, Caviana, and Mexiana Islands possess color patterns of Alouatta belzebul,while Alouatta seniculusis confirmed as the species that inhabits Gurupá Island. The high variability of pelage coloration of the animals from Marajó, Caviana, and Mexiana Islands includes all phenotypes formerly designated as different subspecies. The howler populations from these three islands belong to the same subspecies as those populations that inhabit the region of Tucurui dam reservoir (area 4). Finally, it seems that, as also suggested by chromosome studies, A. belzebulprobably comprises different epiphenotypes without taxonomic validity.     

Genetic markers distinguishing between the two subspecies of the rosy bitterling,Rhodeus ocellatus (Cyprinidae)

Eleven populations of the rosy bitterling,Rhodeus ocellatus, from different localities in Japan, were genetically compared at 16 protein-coding loci using starch-gel electrophoresis. Two loci,Ldh-2 andPgdh, were demonstrated as diagnostic markers for the identification of two subspecies;R. ocellatus kurumeus, which is native to Japan, andR. ocellatus ocellatus, which was introduced from China. The two subspecies were distinguished by the complete substitution of different alleles between them. Population ofR. ocellatus kurumeus occurring in Yao City, Osaka, and in Kanzaki, Saga Prefecture were genetically closely related to each other (genetic distance: D=0.056) but distantly so toR. ocellatus ocellatus from Saitama Prefecture (D=0.202 or 0.265). Electrophoretic analyses also elucidated the existence of hybrid populations of the two subspecies. The populations ofR. ocellatus kurumeus in Yao City had lower genetic variability and a lower incidence of white coloration on the ventral fins than populations of the same in Saga Prefecture. The present study strongly implies that the introduction of the foreign freshwater fishes with subspecific differentiation, into the original range of indigenous subspecies, should be averted not to bring the genetic pollution.     

Intra- and interspecific variation in body size ofProtohermes (Megaloptera: Corydalidae)

The life history of three populations ofProtohermes grandis and two populations ofProtohermes immaculatus (Megaloptera: Corydalidae) was compared. In general, the larvae lived in stream riffles for 2 years and the adults appeared in summer. Adult body size differed between these closely related species and also between the populations ofP. grandis. Dwarfism occurred inP. immaculatus, a species that is endemic to the small, isolated island, Amami Island. The population ofP. grandis on Yaku Island, located between Amami Island and the mainland Kyushu, had an intermediate body size between that ofP. immaculatus and the mainland population ofP. grandis. Despite being an insular population,P. grandis on Tsushima Island had a similar body size to mainlandP. grandis. In these populations with large adults, some larvae lived in the streams for 3 years. The size distribution of benthic animals, which are the prey available toProtohermes larvae, differed between the streams studied. The density of large prey was lowest on Amami Island, intermediate on Yaku Island, and highest on the mainland and Tsushima Island. Different size distributions of available prey may be caused by the differences of benthic fauna; most of Ecdyonuridae and Ephemerellidae (large mayflies) and Perlidae (large stoneflies) were not found on Amami and Yaku Islands. Thus, there is a tendency to dwarfism in the populations ofProtobermes inhabiting streams where the density of large prey is low.     

Size,shape and sex differences in three subspecies of Black-tailed Godwits Limosa limosa

ABSTRACT

Capsule: Black-tailed Godwits Limosa limosa show sexual size dimorphism and size differences between the subspecies. The shape varies slightly between the subspecies, but not between the sexes.

Aims: To investigate whether and how the three subspecies of Black-tailed Godwits, and the sexes of these subspecies, differ in size and shape.

Methods: We collected body dimensions (lengths of the bill, total head, tarsus, tarsus-toe and wing) of adult Black-tailed Godwits from three locations (Iceland, the Netherlands and northwest Australia) corresponding to the breeding or wintering grounds of three known subspecies (islandica, limosa and melanuroides, respectively). Determining sex by molecular assays, we computed degrees of sexual size dimorphism. Using principal component analysis (PCA), we compared differences in size and shape among the different subspecies.

Results: The limosa subspecies was the largest and also showed the most significant sexual size dimorphism. Sexual size dimorphism was smallest for wing length and largest for bill length. The first two axes of the PCA that included all subspecies of both sexes explained 94% of the total variation. Most body dimensions were highly correlated with each other, but wing length varied independently of the other dimensions. Males and females differed only in size (the first axis). However, one of the two small subspecies, islandica, also differed in shape (the second axis) from limosa and melanuroides.

Conclusions: In all three subspecies of Black-tailed Godwits, females are larger than males. The fact that subspecies differed in the degree of size dimorphism and slightly in shape hints at sex-related differences in the ecological selection pressures between the different flyways.     

Plasticity or fixed adaptive traits? Strategies for predation avoidance in Rana arvalis tadpoles

Tadpoles of Rana arvalis originating from seven island populations were tested for responses to non-lethal predator presence. In general, tadpole growth was reduced and the relative tail depth was increased at predator presence. There was no effect of predator presence on the predicted size at metamorphosis. The differentiation rate, translating as length of the larval period, was lower at predator presence, but this seems to be merely an effect of the reduced growth. Although populations differed with respect to growth, relative tail length, relative tail depth, differentiation rate and predicted size at metamorphosis, no obvious differences were found in their responses to predator presence. Data on predator occurrences in the source ponds show that tadpoles originating from ponds with a high predation pressure have a higher differentiation rate, i.e. they will metamorphose at an earlier date than those from “safe” ponds (if raised under the same conditions). Moreover, they are also predicted to metamorphose at a smaller size, which is in accordance with theoretical models. Despite the fact that populations differed in growth, no correlation was found between growth and predation risk in the source ponds. Received: 16 March 1998 / Accepted: 18 July 1998     

Effects of parentage on competitive ability and vulnerability to predation in Hyla chrysoscelis tadpoles

Four sibships of Hyla chrysoscelis larvae were used to examine the effects of parentage on mass at day 23 of growth and on vulnerability to predation. The H. chrysoscelis larvae were raised alone, in competition with Rana clamitans larvae, and in competition with siblings. Vulnerability to predation by adult Notophthalmus viridescens dorsalis was evaluated for Hyla that had been raised in competition with siblings. Sibships differed in body mass and vulnerability to predation. Competition with Rana or with siblings resulted in a major reduction in body mass. There were no interactions between the effects of parentage and level of competition on body mass. Vulnerability to predation by newts appeared to be determined partially by body mass and partially by parental influences on factors other than body mass. If the differences observed between factors determining body mass and vulnerability to predation reflect negative genetic correlations among these determinants, tradeoffs between selection for increased competitive ability and reduced vulnerability to predators may partially account for the existence of genetic variation for growth rate in larval Hyla.     

Contrasting reproductive parameters ingalago senegalensis braccatus andG. s. moholi

Reproductive parameters were compared between two subspecies of the lesser bushbaby, Galago senegalensis braccatusand G. s. moholi.Adult body weights for both male and female G. s. braccatuswere significantly higher than adult body weights of G. s. moholi,as were infant birth weights. The mean gestation length of G. s. braccatuswas significantly longer than that of G. s. moholi. G. s. moholihad a higher incidence of twinning than G. s. braccatus.Puberty in females occurred significantly later in G. s. braccatusthan in G. s. moholi.These differences are of such magnitude that hybridization of G. s. braccatuswith G. s. moholiwould be unlikely. These differences, if augmented by additional evidence, may warrant distinction of the two subspecies at the species level.