Physiographic and climatic events in the Chihuahuan Desert lead to the speciation and distinct demographic patterns of two sister Sceloporus lizards

The biogeographic history of the Chihuahuan Desert is known to be complex, and there is evidence of the effects of physiographic and climatic events in species diversification and demographic population changes in many taxa. Here, using DNA sequence data, we studied the influence of the physiographic and climatic events that occurred in the Chihuahuan Desert during the Pliocene–Pleistocene transition on the speciation and evolutionary history of the sister lizard species Sceloporus cyanostictus and S. gadsdeni. First, based on mtDNA and nDNA sequences, we estimated the divergence times of the sister species. Then, based on mtDNA sequences, we investigated the demographic history of both species within a phylogeographic framework. The divergence time was inferred to be 1.48 Mya, date that corresponds to the existence of a large lake in the Mapimian subprovince, between the current geographic locations of S. cyanostictus and S. gadsdeni. This lake could have acted as a barrier, leading to the speciation of both species. For the demographic history of the two species, we identified two distinct patterns: the population expansion of S. gadsdeni within the Last Glacial Maximum and the potential population decline of S. cyanostictus. Our results can be used as a guide for the study of other aspects that could be critical to developing conservation actions that ensure the survival of not only S. gadsdeni and S. cyanostictus, but also other co‐occurring lizard species.     

MORPHOLOGICAL DIVERSIFICATION AND ADAPTIVE RADIATION: A COMPARISON OF TWO DIVERSE LIZARD CLADES

We compared the morphological diversity (i.e., the amount of morphological space occupied) of two similar clades, the lizard genera Anolis and Sceloporus. These species-rich monophyletic clades are similar in body size, age of origin, and many aspects of their natural history. We examined a number of morphological traits whose variation is likely to represent adaptation to different aspects of the environment, including body size, limb proportions, head dimensions, and tail length. Examination of the position of species in multidimensional space, based on a principal components analysis, indicates that the morphological diversity of Anolis, which we refer to as disparity, is significantly greater than that of Sceloporus. One potential explanation for this pattern is that morphological diversification in Anolis was facilitated by the evolution of subdigital toe-pads, which allow anoles to use the environment in ways not available to Sceloporus. The geographic location of diversification (tropical and subtropical for Anolis, arid for Sceloporus) may also have been important.     

Rapid divergence of social signal coloration across the White Sands ecotone for three lizard species under strong natural selection

Animal social signals are important for population recognition, communication, and mate choice. Although natural selection often favours cryptic coloration, sexual selection can underlie patterns of coloration that function in inter- or intrasexual communication. We compared social signal coloration of three lizard species across a substrate colour ecotone in New Mexico. These species exhibit cryptic blanched dorsal coloration on the gypsum dunes of White Sands and dark coloration on the surrounding desert soils. We detected corresponding population divergence in colour used for intra- ( Aspidoscelis inornata , Sceloporus undulatus ) or inter- ( Holbrookia maculata ) sexual signalling. Although the magnitude and direction of change in coloration varied among taxa, differences in hue and chroma accounted for more variation in social coloration than for dorsal coloration. The relative conspicuousness of social signals also varied across the ecotone. We discuss the possibilities that divergent signalling colours in this system are the result of: (1) stochastic processes, (2) direct selection, and/or (3) a correlated response to natural selection on dorsal coloration.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 243–255.     

Lizards fail to plastically adjust nesting behavior or thermal tolerance as needed to buffer populations from climate warming

Although observations suggest the potential for phenotypic plasticity to allow adaptive responses to climate change, few experiments have assessed that potential. Modeling suggests that Sceloporus tristichus lizards will need increased nest depth, shade cover, or embryonic thermal tolerance to avoid reproductive failure resulting from climate change. To test for such plasticity, we experimentally examined how maternal temperatures affect nesting behavior and embryonic thermal sensitivity. The temperature regime that females experienced while gravid did not affect nesting behavior, but warmer temperatures at the time of nesting reduced nest depth. Additionally, embryos from heat‐stressed mothers displayed increased sensitivity to high‐temperature exposure. Simulations suggest that critically low temperatures, rather than high temperatures, historically limit development of our study population. Thus, the plasticity needed to buffer this population has not been under selection. Plasticity will likely fail to compensate for ongoing climate change when such change results in novel stressors.     

CYTOGENETIC ANALYSIS OF CHROMOSOMAL INTERMEDIATES FROM A HYBRID ZONE BETWEEN TWO CHROMOSOME RACES OF THE SCELOPORUS GRAMMICUS COMPLEX (SAURIA,PHRYNOSOMATIDAE)

Underdominance for chromosomal rearrangements is the central assumption of several models of chromosomally based speciation including the cascade model, proposed for the Sceloporus grammicus complex. Several cytotypes of the S. grammicus complex hybridize at localities in central México. A hybrid zone between two of the most chromosomally divergent races (= cytotypes) of S. grammicus (F5, 2n = 34 and FM2, 2n = 44–46) was examined to assess the meiotic effects of heterozygosity at multiple chromosomes. Meiosis was examined in males heterozygous for “simple” Robertsonian fissions at chromosomes 1, 3, 4, and 6 and/or a pericentric inversion at chromosome 4. Analysis of synaptonemal complexes and chromosomal configurations at diakinesis showed trivalent formation in fission heterozygotes and heterosynapsis (lack of reverse-loop formation) in an inversion heterozygote. Analysis of metaphase II configurations revealed primarily balanced segregation and low levels of nondisjunction regardless of chromosomal background. The lack of underdominance associated with “simple” fission heterozygosity in this narrow hybrid zone contradicts the key premise of most chromosomally based models of speciation.     

FEMALE FECUNDITY IN A HYBRID ZONE BETWEEN TWO CHROMOSOME RACES OF THE SCELOPORUS GRAMMICUS COMPLEX (SAURIA,PHRYNOSOMATIDAE)

Individuals of the F5 and FM2 cytotypes of the Sceloporus grammicus complex form a narrow zone of parapatric hybridization near Tulancingo, Hidalgo, Mexico. Reproductive parameters were examined among chromosomally parental and hybrid females to assess the degree to which reduced clutch size is correlated with the level of chromosomal heterozygosity. Although clutch size in the two parental groups was highly correlated with female body size, this was not the case for females with intermediate karyotypes. These females displayed increased levels of infertility manifested as smaller clutches and as inviable embryos. F₁ females produced the smallest average clutches and suffered the most precipitous fecundity loss (up to 75%). The number of heterozygous marker chromosomes and heterozygosity at chromosome 2 had significant effects on the number of viable embryos. Analysis of embryo karyotypes revealed the production of triploid offspring and an excess number of embryos heterozygous at chromosome 1. Differences in viability, among females heterozygous for the same number of chromosomes, suggest that genetic background of the female and/or sire may be an important factor in determining reproductive success.     

Age determination in the blackfly Simulium woodi, a vector of onchocerciasis in Tanzania

Abstract. Age-dependent changes in the ovarioles of Simulium woodi (Diptera: Simuliidae) and the age structure of a wild population of this species in the Amani hills of north-eastern Tanzania were studied using the ovarian oil injection technique. Contrary to previous theories, egg sacs degenerate completely and do not form dilatations. The physiological age of the females could be determined only by gonotrophic dilatations formed from degenerating follicles during gonotrophic cycles. In individual females, the proportions of ovarioles with degenerating follicles were 3–54% (mean 22%) in the first cycle and 8–61% (mean 36%) in the second gonotrophic cycle. Agonotrophic degenerating follicles occurred in 2% of ovarioles in 12% of females. Additional information with regard to the degree of parity is given by the level of granulation in the basal body of each ovariole, a group of six to eight cells in the calyx wall enclosed by the end of the ovariolar sheath. Their granulation progressively increased in intensity following each subsequent ovulation.     

The consequences of lifetime and evolutionary exposure to toxic prey: changes in avoidance behaviour through ontogeny

Responses to novel threats (e.g. invasive species) can involve genetic changes or plastic shifts in phenotype. There is controversy over the relative importance of these processes for species survival of such perturbations, but we are realizing they are not mutually exclusive. Native eastern fence lizards (Sceloporus undulatus) have adapted to top-down predation pressure imposed by the invasive red imported fire ant (Solenopsis invicta) via changes in adult (but not juvenile) lizard antipredator behaviour. Here, we examine the largely ignored, but potentially equally important, bottom-up effect of fire ants as toxic prey for lizards. We test how fire ant consumption (or avoidance) is affected by lifetime (via plasticity) and evolutionary (via natural selection) exposure to fire ants by comparing field-caught and laboratory-reared lizards, respectively, from fire ant-invaded and uninvaded populations. More naive juveniles from invaded populations ate fire ants than did adults, reflecting a natural ontogenetic dietary shift away from ants. Laboratory-reared lizards from the invaded site were less likely to eat fire ants than were those from the uninvaded site, suggesting a potential evolutionary shift in feeding behaviour. Lifetime and evolutionary exposure interacted across ontogeny, however, and field-caught lizards from the invaded site exhibited opposite ontogenetic trends; adults were more likely to eat fire ants than were juveniles. Our results suggest that plastic and evolutionary processes may both play important roles in permitting species survival of novel threats. We further reveal how complex interactions can shape adaptive responses to multimodal impacts imposed by invaders: in our system, fire ants impose stronger bottom-up selection than top-down selection, with each selection regime changing differently across lizard ontogeny.     

Fluctuations in the incubation moisture environment affect growth but not survival of hatchling lizards

Few studies have collected longitudinal data that follow the complete microevolutionary path of an organism linking sources of variation (e.g. environmental versus genetic) to a trait and its subsequent relationship with fitness. Identifying the links within this pathway is imperative for understanding the ecological relevance of effects found at the phenotypic level. Furthermore, experimental studies that examine parts of the pathway in ectothermic organisms often fail to mimic the complexities of the natural developmental environment. Temperature and moisture conditions in reptile nests, for example, can fluctuate greatly on a seasonal and daily basis. Despite the potential effects of fluctuating environments, the vast majority of studies have held environmental treatments constant during the developmental period. We investigated the effects of fluctuating moisture regimes during incubation on eggs, hatchling phenotypes, and subsequent survival in the eastern fence lizard Sceloporus undulatus. Moisture fluctuations during embryonic development caused water absorption by eggs to follow the environmental availability of moisture. Initial hatchling tail length was affected by the pattern of moisture fluctuations, and hatchling growth rates in fluctuating treatments were significantly faster than those in a constant treatment, resulting in larger hatchlings after 4 weeks. A release–recapture experiment conducted in the field did not detect a treatment effect on survival despite the larger body sizes. In summary, although fluctuations affected water absorption by eggs and some hatchling traits, these effects did not have subsequent fitness consequences. The results obtained suggest that egg and hatchling survival are buffered against natural soil moisture fluctuations during incubation, even when egg and hatchling traits are significantly affected. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 89–102.