Paul Doughty

Divergent Selection and the Evolution of Signal Traits and Mating Preferences

Mating preferences are common in natural populations, and their divergence among populations is considered an important source of reproductive isolation during speciation. Although mechanisms for the divergence of mating preferences have received substantial theoretical treatment, complementary experimental tests are lacking. We conducted a laboratory evolution experiment, using the fruit fly Drosophila serrata, to explore the role of divergent selection between environments in the evolution of female mating preferences. Replicate populations of D. serrata were derived from a common ancestor and propagated in one of three resource environments: two novel environments and the ancestral laboratory environment. Adaptation to both novel environments involved changes in cuticular hydrocarbons, traits that predict mating success in these populations. Furthermore, female mating preferences for these cuticular hydrocarbons also diverged among populations. A component of this divergence occurred among treatment environments, accounting for at least 17.4% of the among-population divergence in linear mating preferences and 17.2% of the among-population divergence in nonlinear mating preferences. The divergence of mating preferences in correlation with environment is consistent with the classic by-product model of speciation in which premating isolation evolves as a side effect of divergent selection adapting populations to their different environments.

Detecting life history trade-offs: measuring energy stores in “capital” breeders reveals costs of reproduction

Abstract Life history trade-offs should be detectable as negative correlations between the relevant traits (e.g. reproductive output versus energy storage), but may be masked by variation in resource levels among individuals. One way to detect underlying trade-offs, at least in organisms that rely on stored energy for reproduction (“capital breeders”), may be to monitor an individuals energy stores before and after reproduction. We analysed energy stores and reproductive output in Eulamprus tympanum, a viviparous scincid lizard that stores energy for reproduction in its tail. One predicted trade-off (that between the size and number of offspring in a litter) is consistently observed, and is detectable with minimal information. Another predicted trade-off (that between offspring size and subsequent energy reserves) is not apparent in our data, perhaps because of constraints imposed by correlations among other traits. Finally, trade-offs between reproductive output and subsequent energy stores are evident in this species, but are only detectable with information on the extent of pre-reproductive as well as post-reproductive energy stores. For “capital breeders”, non-destructive measurement of pre- and post-reproductive energy stores may greatly enhance our ability to detect significant life history trade-offs.

REPRODUCTIVE ENERGY ALLOCATION AND LONG‐TERM ENERGY STORES IN A VIVIPAROUS LIZARD (EULAMPRUS TYMPANUM)

When animals reproduce, does energy for the brood come from stored re- serves (from food eaten months or years before), or from food eaten during the current reproductive season? Variation in the duration of energy storage prior to reproduction is an important, but little-studied, axis of life history variation. We experimentally manipulated the availability of resources to females of a long-lived viviparous lizard (Eulamprus tym- panum. Scincidae) in the first year of a two-year study to assess the relative importance of current food intake vs. stored reserves as sources of energy for breeding. Females given greater access to high temperatures (and hence, to resources) in the laboratory amassed larger caudal energy stores than did females with lesser opportunities. Energy intake during gestation slightly influenced offspring size, but the magnitude of energy stores prior to ovulation had a more dramatic effect: females with larger caudal energy stores produced much larger litters in the following year. Growth rates of females were unaffected by basking treatments or by reproduction in either year, but females that reproduced in the second year showed a large concomitant decrease in caudal energy stores compared to females that did not reproduce, indicating a large energetic cost of reproduction. Hence, reproductive output within this species can be influenced by resource availability over 12 months prior to reproduction, and simple comparisons of reproductive output with current resource avail- ability may fail to detect the ways in which phenotypically plastic life history traits are influenced by environmental features. In addition to an appropriate temporal framework, models of resource allocation should also incorporate the possible roles of physiological and morphological constraints (e.g., maternal inability, in some species, to modify post- ovulation reproductive expenditure) and trade-offs with other life history currencies (e.g., decrements in maternal survival due to high relative clutch masses). The time lag between resource acquisition and expenditure may have significant consequences for a populations demographic response to shifts in resource availability or predation pressure (via tail au- totomy). Finally, this study illustrates the way in which thermal aspects of the environment can influence life history phenotypes in ectothermic vertebrates with long-term energy stores.

Cryptic diversity in vertebrates: molecular data double estimates of species diversity in a radiation of Australian lizards (Diplodactylus, Gekkota)

A major problem for biodiversity conservation and management is that a significant portion of species diversity remains undocumented (the ‘taxonomic impediment’). This problem is widely acknowledged to be dire among invertebrates and in developing countries; here, we demonstrate that it can be acute even in conspicuous animals (reptiles) and in developed nations (Australia). A survey of mtDNA, allozyme and chromosomal variation in the Australian gecko, genus Diplodactylus, increases overall species diversity estimates from 13 to 29. Four nominal species each actually represent multi-species complexes; three of these species complexes are not even monophyletic. The high proportion of cryptic species discovered emphasizes the importance of continuing detailed assessments of species diversity, even in apparently well-known taxa from industrialized countries.

Synchronous polyandry and multiple paternity in the frog Crinia georgiana (Anura: Myobatrachidae)

Multiple paternity has rarely been reported in anuran amphibians, with only three previous documented examples. For the Australian frog Crinia georgiana, we observed synchronous polyandry in an average of 44% of matings observed at four field sites. This suggests matings involving more than one male are common in this species. One to eight males were observed in amplectant groups with second males amplexed ventrally. Genetic analyses, using allozyme electrophoresis, of offspring from two matings indicated that at least two of three possible males fathered offspring. Third males were unlikely to have shared paternity, explained by their inappropriate position during amplexus. Multiple paternity may be more common in frogs than has been reported. Copyright 1999 The Association for the Study of Animal Behaviour.

Male choice generates stabilizing sexual selection on a female fecundity correlate

We know very little about male mating preferences and how they influence the evolution of female traits. Theory predicts that males may benefit from choosing females on the basis of traits that indicate their fecundity. Here, we explore sexual selection generated by male choice on two components of female body size (wing length and body mass) in Drosophila serrata. Using a dietary manipulation to alter female size and 828 male mate choice trials, we analysed linear and nonlinear sexual selection gradients on female mass and wing length. In contrast to theoretical expectations and prevailing empirical data, males exerted stabilizing rather than directional sexual selection on female body mass, a correlate of fecundity. Sexual selection was detected only among females with access to standard resource levels as an adult, with no evidence for sexual selection among resource‐depleted females. Thus the mating success of females with the same body mass differed depending upon their access to resources as an adult. This suggests that males in this species may rely on signal traits to assess body mass rather than assessing it directly. Stabilizing rather than directional sexual selection on body mass together with recent evidence for stabilizing sexual selection on candidate signal traits in this species suggests that females may trade‐off resources allocated to reproduction and sexual signalling.

Energetic costs of tail loss in a montane scincid lizard

Most species of lizards will shed their tails at the point of contact when grasped by a predator. We investigated the energetic consequences of tail loss by measuring lipids in a scincid lizard that stores energy in its tail for reproduction. Most of the lipids were concentrated in the proximal portion of the tail. Thus, partial tail loss may not severely affect energy stores if the distal portion of the tail is shed in predatory encounters. We also found that the width of the tail was a reliable non-invasive index of energy reserves in this species.

EXPERIMENTAL EVIDENCE OF AN AGE-SPECIFIC SHIFT IN CHEMICAL DETECTION OF PREDATORS IN A LIZARD

The risk posed by predation is one of the most fundamental aspects of an animals environment. Avoidance of predators implies an ability to obtain reliable information about the risk of predation, and for many species, chemosensory cues are likely to be an important source of such information. Chemosensory cues reliably reveal the presence of predators or their presence in the recent past. We used retreat site selection experiments to test whether the Australian scincid lizard EulamprusheatwoleiM uses chemical cues for predator detection and avoidance. Both adult and juvenile lizards were given the choice of retreat sites treated with scents from invertebrate predators, as well as sympatric and allopatric snake predators. Some of the snake predators were known to eat E. heatwolei, while others did not pose a predation threat. All invertebrate predators posed a risk to juveniles, but not adults because of their size. We found that juvenile E. heatwolei avoided predator odors more strongly than adults. Juveniles avoided both invertebrate predators and snakes, and the strongest response was toward the funnelweb spider, the only ambush predator used in this experiment. This result may demonstrate the importance of predator ecology in the evolution of predator detection mechanisms, with chemical cues being more useful in detecting sedentary predators than active predators. Adult lizards showed no avoidance behavior toward predator odors. This result suggests an age specific shift in predator avoidance behavior as lizards get older and become too large for many predators. However, adults showed no response to the odor from the red-bellied black snake, a known predator of adult E. heatwolei. This finding further demonstrates the importance of predator ecology when examining communication between predators and prey. Chemical cues, which are persistent long after predators have vacated the area, may not be useful in detecting the red-bellied black snake, a wide-ranging active forager.

Plasticity in age and size at metamorphosis of Crinia georgiana tadpoles: responses to variation in food levels and deteriorating conditions during development

Adaptive phenotypic plasticity in life-history traits is predicted to evolve when populations occur in heterogeneous environments. Anuran larvae of many species cannot escape their aquatic environment until metamorphosis and therefore should show plasticity in response to conditions experienced as tadpoles. In this study, we manipulated the aquatic environments of Crinia georgiana tadpoles in the laboratory to mimic variation among ponds in resources and drying conditions in nature. This species breeds in very shallow water in winter and ponds frequently dry between bouts of rain, especially towards spring. Tadpoles kept in constant conditions at different levels of food metamorphosed at different body sizes but showed no plasticity in metamorphic timing. Tadpoles fed only lettuce metamorphosed at sizes similar to those of field-collected tadpoles, whereas tadpoles fed a more protein-rich food metamorphosed at unusually large sizes, indicating that the seeps where C. georgiana tadpoles occur are poor in nutrients. When we decreased food and water levels, tadpoles at later developmental stages were able to accelerate development and metamorphose earlier than tadpoles kept under constant conditions. Furthermore, tadpoles in very shallow water with no access to food metamorphosed earlier and at smaller body sizes than tadpoles with a more moderate decrease in depth that were able to continue feeding. Rapid development and the ability to accelerate metamorphosis in C. georgiana tadpoles are consistent with adaptation in a heterogeneous environment where larvae are under strong time constraints.

Hidden biodiversity in rare northern Australian vertebrates: the case of the clawless geckos (Crenadactylus, Diplodactylidae) of the Kimberley

Abstract Context. The phylogenetic diversity and biogeography of most animal and plant lineages endemic to the Australian Monsoonal tropics remains poorly understood. Of particular note (and in contrast to many other tropical regions in both Australia and elsewhere) is the current paucity of evidence for diverse endemic radiations of restricted-range taxa. Aims. To use recently collected material from major surveys of the Kimberley Islands, Western Australia, to expand on a previous study that provided preliminary evidence of very high levels of geographically structured phylogenetic diversity in a lineage of tiny geckos (Crenadactylus). Methods. Mitochondrial (ND2) and nuclear (RAG-1) sequence data were used to estimate the relationships, phylogenetic diversity and timescale of diversification of all populations of Crenadactylus from northern Australia from which samples for genetic analysis were available. Key results. In striking contrast to the two subspecies currently recognised in the Kimberley, our analyses confirm the existence of a notable diversity of highly divergent and apparently allopatric lineages within the Kimberley, including at least 10 that are estimated to date to the late Pliocene/early Miocene (or earlier) and seven that we recognise as candidate new species. Most of this diversity is concentrated in the high-rainfall zone along the western edge of the Kimberley. Key conclusions. A growing number of genetic datasets are revealing northern Australian vertebrate clades characterised by the juxtaposition of deeply divergent and highly geographically structured genetic diversity on the one hand, and major geographic gaps in sampling that impede full assessment of the distribution and taxonomic significance of this diversity on the other. Implications. There is a pressing need for further surveys, voucher material and phylogenetic analyses to allow us to properly understand the diversity, biogeography and conservation needs of the northern Australian biota.