Stewart L. Macdonald

Heat hardening in a tropical lizard: geographic variation explained by the predictability and variance in environmental temperatures

Over the coming decades, our planet will experience a dramatic increase in average temperatures and an increase in the variance around those temperatures leading to more frequent and harsher heat waves. These changes will impact most species and impose strong selection on physiological traits. Rapid acclimation is the most direct way for organisms to respond to such extreme events, but we currently have little understanding of how the capacity to mount such plastic responses evolves. Accordingly, there is some urgency to determine how the physiological response to high temperatures varies within species, and how this variation is driven by the environment. Here, we investigate heat-hardening capacity - a rapid physiological response that confers a survival advantage under extreme thermal stress - across 13 populations of a rain forest lizard, Lampropholis coggeri, from the tropics of north-eastern Australia. Our results reveal that heat hardening is constrained in these lizards by a hard upper thermal limit for locomotor function (approximately 43 degrees C). Further, hardening response shows strong geographic variation associated with thermal environment: lizards from more predictable and more seasonal thermal environments exhibited greater hardening compared with those from more stochastic and less seasonal habitats. This finding - that predictability in thermal variation influences hardening capacity - aligns closely with theoretical expectations. Our results suggest that tropical species may harbour adaptive variation in physiological plasticity that they can draw from in response to climate change, and this variation is spatially structured in locally adapted populations. Our results also suggest that, by using climatic data, we can predict which populations contain particular adaptive variants; information critical to assisted gene flow strategies.

Do evolutionary constraints on thermal performance manifest at different organizational scales

The two foremost hypotheses on the evolutionary constraints on an organisms thermal sensitivity – the hotter‐is‐better expectation, and the specialist–generalist trade‐off – have received mixed support from empirical studies testing for their existence. Could these conflicting results reflect confusion regarding the organizational level (i.e. species > population > individual) at which these constraints should manifest? We propose that these evolutionary constraints should manifest at different organizational levels because of differences in their underlying causes and requirements. The hotter‐is‐better expectation should only manifest across separate evolutionary units (e.g. species, populations), and not within populations. The specialist–generalist trade‐off, by contrast, should manifest within as well as between separate evolutionary units. We measured the thermal sensitivity of sprint performance for 440 rainforest sun skinks (Lampropholis coggeri) representing 10 populations, and used the resulting performance curves to test for evidence for the hypothesized constraints at two organizational levels: (i) across populations and (ii) within populations. As predicted, the hotter‐is‐better expectation was evident only at the across‐population level, whereas the specialist–generalist trade‐off was evident within, as well as across, populations. Our results suggest that, depending on the processes that drive them, evolutionary constraints can manifest at different organizational levels. Consideration of these underlying processes, and the organizational level at which a constraint should manifest, may help resolve conflicting empirical results.

Peripheral isolates as sources of adaptive diversity under climate change

As climate change progresses, there is increasing focus on the possibility of using targeted gene flow (the movement of pre-adapted individuals into declining populations) as a management tool. Targeted gene flow is a relatively cheap, low-risk management option and will almost certainly come into increased use over the coming decades. Before such action can be taken, however, we need to know where to find pre-adapted individuals. We argue that, for many species, the obvious place to look for this diversity is in peripheral isolates: isolated populations at the current edges of a species’ range. Both evolutionary and ecological considerations suggest that the bulk of a species’ adaptive variation may be contained in the total set of these peripheral isolates. Moreover, by exploring both evolutionary and ecological perspectives it becomes clear that we should be able to assess the potential value of each isolate using remotely sensed data and three measurable axes of variation in patch traits: population size, connectivity, and climatic environment. Locating the “sweet spot” in this trait space, however, remains a challenge. Throughout, we illustrate these ideas using Australia’s Wet Tropics rainforests as a model system.

Gross morphology and microstructure of type locality ossicles of Psephophorus polygonus Meyer, 1847 (Testudines, Dermochelyidae)

Psephophorus polygonus Meyer, 1847, the first fossil leatherback turtle to be named, was described on the basis of shell ossicles from the middle Miocene (MN6-7/8?) of Slovakia. The whereabouts of this material is uncertain but a slab on display at the Naturhistorisches Museum Wien is considered the neotype. We rediscovered further type locality ossicles in four European institutions, re-evaluated their gross morphology and described for the first time their microstructure by comparing them with Dermochelys coriacea, the only living dermochelyid turtle. The gross morphology is congruent with that already described for P. polygonus, but with two significant exceptions: the ridged ossicles of P. polygonus may have a distinctly concave ventral surface as well as a tectiform shape in cross-section. They do not develop the external keel typical of many ossicles of D. coriacea. Both ridged and non-ridged ossicles of P. polygonus are characterized by compact diploe structures with an internal cortex consisting of a coarse fibrous meshwork, whereas the proportionately thinner ossicles of D. coriacea tend to lose the internal cortex, and thus their diploe, during ontogeny. The ossicles of both P. polygonus and D. coriacea differ from those of other lineages of amniotes whose carapace is composed of polygonal ossicles or platelets, in having growth centres situated at the plate centres just interior to the external bone surface and not within the cancellous core or closer to the internal compact layer. The new diagnosis of P. polygonus allows us to preliminarily re-evaluate the taxonomy of some of the Psephophorus-like species. Despite some macro-and micromorphological differences, it seems likely that Psephophorus was as cosmopolitan as extant Dermochelys and had a broadly similar ecology, with a possible difference concerning the dive depth.

Using connectivity to identify climatic drivers of local adaptation

Understanding the climatic drivers of local adaptation is vital. Such knowledge is not only of theoretical interest but is critical to inform management actions under climate change, such as assisted translocation and targeted gene flow. Unfortunately, there are a vast number of potential trait-environment combinations, and simple relationships between trait and environment are ambiguous: representing either plastic or evolved variation. Here, we show that by incorporating connectivity as an index of gene flow, we can differentiate trait-environment relationships reflecting genetic variation vs. phenotypic plasticity. In this way, we rapidly shorten the list of trait-environment combinations that are of significance. Our analysis of an existing data set on geographic variation in a tropical lizard shows that we can effectively rank climatic variables by the strength of their role in local adaptation. The promise of our method is a rapid and general approach to identifying the environmental drivers of local adaptation.

Adjusting to climate: Acclimation, adaptation and developmental plasticity in physiological traits of a tropical rainforest lizard

The impact of climate change may be felt most keenly by tropical ectotherms. In these taxa, it is argued, thermal specialization means a given shift in temperature will have a larger effect on fitness. For species with limited dispersal ability, the impact of climate change depends on the capacity for their climate-relevant traits to shift. Such shifts can occur through genetic adaptation, various forms of plasticity, or a combination of these processes. Here we assess the extent and causes of shifts in 7 physiological traits in a tropical lizard, the rainforest sunskink (Lampropholis coggeri). Two populations were sampled that differ from each other in both climate and physiological traits. We compared trait values in each animal soon after field collection versus following acclimation to laboratory conditions. We also compared trait values between populations in: (i) recently field-collected animals; (ii) the same animals following laboratory acclimation; and (iii) the laboratory-reared offspring of these animals. Our results reveal high trait lability, driven primarily by acclimation and local adaptation. By contrast, developmental plasticity, resulting from incubation temperature, had little to no effect on most traits. These results suggest that, while specialized, tropical ectotherms may be capable of rapid shifts in climate-relevant traits.