Gregory P. Brown

An evolutionary process that assembles phenotypes through space rather than through time

In classical evolutionary theory, traits evolve because they facilitate organismal survival and/or reproduction. We discuss a different type of evolutionary mechanism that relies upon differential dispersal. Traits that enhance rates of dispersal inevitably accumulate at expanding range edges, and assortative mating between fast-dispersing individuals at the invasion front results in an evolutionary increase in dispersal rates in successive generations. This cumulative process (which we dub “spatial sorting”) generates novel phenotypes that are adept at rapid dispersal, irrespective of how the underlying genes affect an organisms survival or its reproductive success. Although the concept is not original with us, its revolutionary implications for evolutionary theory have been overlooked. A range of biological phenomena (e.g., acceleration of invasion fronts, insular flightlessness, preadaptation) may have evolved via spatial sorting as well as (or rather than) by natural selection, and this evolutionary mechanism warrants further study.

Life-history evolution in range-shifting populations

Most evolutionary theory does not deal with populations expanding or contracting in space. Invasive species, climate change, epidemics, and the breakdown of dispersal barriers, however, all create populations in this kind of spatial disequilibrium. Importantly, spatial disequilibrium can have important ecological and evolutionary outcomes. During continuous range expansion, for example, populations on the expanding front experience novel evolutionary pressures because frontal populations are assorted by dispersal ability and have a lower density of conspecifics than do core populations. These conditions favor the evolution of traits that increase rates of dispersal and reproduction. Additionally, lowered density on the expanding front eventually frees populations on the expanding edge from specialist, coevolved enemies, permitting higher investment into traits associated with dispersal and reproduction rather than defense against pathogens. As a result, the process of range expansion drives rapid life-history evolution, and this seems to occur despite ongoing serial founder events that have complex effects on genetic diversity at the expanding front. Traits evolving on the expanding edge are smeared across the landscape as the front moves through, leaving an ephemeral signature of range expansion in the life-history traits of a species across its newly colonized range. Recent studies suggest that such nonequilibrium processes during recent population history may have contributed to many patterns usually ascribed to evolutionary forces acting in populations at spatial equilibrium.

Reid's paradox revisited: the evolution of dispersal kernels during range expansion.

Current approaches to modeling range advance assume that the distribution describing dispersal distances in the population (the “dispersal kernel”) is a static entity. We argue here that dispersal kernels are in fact highly dynamic during periods of range advance because density effects and spatial assortment by dispersal ability (“spatial selection”) drive the evolution of increased dispersal on the expanding front. Using a spatially explicit individual‐based model, we demonstrate this effect under a wide variety of population growth rates and dispersal costs. We then test the possibility of an evolved shift in dispersal kernels by measuring dispersal rates in individual cane toads (Bufo marinus) from invasive populations in Australia (historically, toads advanced their range at 10 km/year, but now they achieve >55 km/year in the northern part of their range). Under a common‐garden design, we found a steady increase in dispersal tendency with distance from the invasion origin. Dispersal kernels on the invading front were less kurtotic and less skewed than those from origin populations. Thus, toads have increased their rate of range expansion partly through increased dispersal on the expanding front. For accurate long‐range forecasts of range advance, we need to take into account the potential for dispersal kernels to be evolutionarily dynamic.

Adapting to the unpredictable: reproductive biology of vertebrates in the Australian wet-dry tropics.

In the wet–dry tropics of northern Australia, temperatures are high and stable year-round but monsoonal rainfall is highly seasonal and variable both annually and spatially. Many features of reproduction in vertebrates of this region may be adaptations to dealing with this unpredictable variation in precipitation, notably by (i) using direct proximate (rainfall-affected) cues to synchronize the timing and extent of breeding with rainfall events, (ii) placing the eggs or offspring in conditions where they will be buffered from rainfall extremes, and (iii) evolving developmental plasticity, such that the timing and trajectory of embryonic differentiation flexibly respond to local conditions. For example, organisms as diverse as snakes (Liasis fuscus, Acrochordus arafurae), crocodiles (Crocodylus porosus), birds (Anseranas semipalmata) and wallabies (Macropus agilis) show extreme annual variation in reproductive rates, linked to stochastic variation in wet season rainfall. The seasonal timing of initiation and cessation of breeding in snakes (Tropidonophis mairii) and rats (Rattus colletti) also varies among years, depending upon precipitation. An alternative adaptive route is to buffer the effects of rainfall variability on offspring by parental care (including viviparity) or by judicious selection of nest sites in oviparous taxa without parental care. A third type of adaptive response involves flexible embryonic responses (including embryonic diapause, facultative hatching and temperature-dependent sex determination) to incubation conditions, as seen in squamates, crocodilians and turtles. Such flexibility fine-tunes developmental rates and trajectories to conditions–-especially, rainfall patterns–-that are not predictable at the time of oviposition.

Evolutionarily accelerated invasions: the rate of dispersal evolves upwards during the range advance of cane toads.

Human activities are changing habitats and climates and causing species’ ranges to shift. Range expansion brings into play a set of powerful evolutionary forces at the expanding range edge that act to increase dispersal rates. One likely consequence of these forces is accelerating rates of range advance because of evolved increases in dispersal on the range edge. In northern Australia, cane toads have increased their rate of spread fivefold in the last 70 years. Our breeding trials with toads from populations spanning the species’ invasion history in Australia suggest a genetic basis to dispersal rates and interpopulation genetic variation in such rates. Toads whose parents were from the expanding range front dispersed faster than toads whose parents were from the core of the range. This difference reflects patterns found in their field‐collected mothers and fathers and points to heritable variance in the traits that have accelerated the toads’ rate of invasion across tropical Australia over recent decades. Taken together with demonstrated spatial assortment by dispersal ability occurring on the expanding front, these results point firmly to ongoing evolution as a driving force in the accelerated expansion of toads across northern Australia.

MATERNAL NEST-SITE CHOICE AND OFFSPRING FITNESS IN A TROPICAL SNAKE (TROPIDONOPHIS MAIRII , COLUBRIDAE)

Do reproducing female reptiles adaptively manipulate phenotypic traits of their offspring by selecting appropriate nest sites? Evidence to support this hypothesis is indirect, mostly involving the distinctive characteristics of used (vs. available) nest sites, and the fact that physical conditions during egg incubation can modify hatchling phenotypic traits that plausibly might influence fitness. Such data fall well short of demonstrating that nesting females actively select from among potential sites based on cues that predict fitness- determining phenotypic modifications of their offspring. We provide such data from ex- perimental studies on a small oviparous snake (the keelback, Tropidonophis mairii) from the wet-dry tropics of Australia. When presented with a choice of alternative nesting sites, egg-laying females selected more moist substrates for egg deposition. Incubation on wetter substrates significantly increased body size at hatching, a trait under strong positive selection in this population (based on mark-recapture studies of free-ranging hatchlings). Remark- ably, the hydric conditions experienced by an egg in the first few hours after it was laid substantially affected phenotypic traits (notably, muscular strength) of the hatchling that emerged from that egg 10 weeks later. Thus, our data provide empirical support for the hypothesis that nesting female reptiles manipulate the phenotypic traits of their offspring through nest-site selection, in ways that enhance offspring fitness.

Comparisons through time and space suggest rapid evolution of dispersal behaviour in an invasive species

During a biological invasion, we expect that the expanding front will increasingly become dominated by individuals with better dispersal abilities. Over many generations, selection at the invasion front thus will favour traits that increase dispersal rates. As a result of this process, cane toads (Bufo marinus) are now spreading through tropical Australia about 5-fold faster than in the early years of toad invasion; but how have toads changed to make this happen? Here we present data from radio-tracking of free-ranging cane toads from three populations (spanning a 15-year period of the toads’ Australian invasion, and across 1800 km). Our data reveal dramatic shifts in behavioural traits (proportion of nights when toads move from their existing retreat-site to a new one, and distance between those successive retreat-sites) associated with the rapid acceleration of toad invasion. Over a maximum period of 70 years (~50 generations), cane toads at the invasion front in Australia apparently have evolved such that populations include a higher proportion of individuals that make long, straight moves.

Reproductive ecology of a tropical natricine snake, Tropidonophis mairii (Colubridae)

Although most snake species are tropical, very little is known about their biology. We monitored reproductive histories of individually marked natricine colubrid snakes (keelbacks, Tropidonophis mairii) for 18-months in a tropical Australian floodplain. Our data provide the first unambiguous records (for any snake species) of individual females in a natural population producing multiple clutches of eggs during a single breeding season. The snakes bred throughout drier months of the year. The mean size of reproducing females decreased over the season, whereas relative clutch mass increased significantly over the same time period. Larger females produced eggs that were not only larger, but also shorter and wider, than those of smaller females. Despite producing two clutches in short succession, female keelbacks grew over the intervening period. Thus, they switch from ‘capital breeding’ (building up stores of energy during the wet season to use for reproduction in the dry season) to ‘income breeding’ (relying on recently ingested energy to support both growth and reproduction during the dry season). Two females marked at hatching were recaptured as breeding adults <12 months later, confirming that maturation is attained more rapidly in this species than in temperate-zone natricines.

Invasion, stress, and spinal arthritis in cane toads

The impact of invasive species on biodiversity has attracted considerable study, but impacts of the invasion process on the invaders themselves remain less clear. Invading species encounter conditions different from those in their ancestral habitats and are subject to intense selection for rapid dispersal. The end result may be significant stress on individual organisms, with consequent health problems. Our studies on invasive cane toads in Australia reveal severe spinal arthritis in ≈10% of large adult toads, associated with the same factors (large body size, frequent movement, and relatively long legs) that have enabled toads to invade so rapidly across the Australian tropics.

WHY DO MOST TROPICAL ANIMALS REPRODUCE SEASONALLY? TESTING HYPOTHESES ON AN AUSTRALIAN SNAKE

Most species reproduce seasonally, even in the tropics where activity occurs year-round. Squamate reptiles provide ideal model organisms to clarify the ultimate (adaptive) reasons for the restriction of reproduction to specific times of year. Females of almost all temperate-zone reptile species produce their eggs or offspring in the warmest time of the year, thereby synchronizing embryogenesis with high ambient temperatures. However, although tropical reptiles are freed from this thermal constraint, most do not reproduce year-round. Seasonal reproduction in tropical reptiles might be driven by biotic factors (e.g., peak periods of predation on eggs or hatchlings, or food for hatchlings) or abiotic factors (e.g., seasonal availability of suitably moist incubation conditions). Keelback snakes (Tropidonophis mairii, Colubridae) in tropical Australia reproduce from April to November, but with a major peak in May-June. Our field studies falsify hypotheses that invoke biotic factors as explanations for this pattern: the timing of nesting does not minimize predation on eggs, nor maximize food availability or survival rates for hatchlings. Instead, our data implicate abiotic factors: female keelbacks nest most intensely soon after the cessation of monsoonal rains when soils are moist enough to sustain optimal embryogenesis (wetter nests produce larger hatchlings, that are more likely to survive) but are unlikely to become waterlogged (which is lethal to eggs). Thus, abiotic factors may favor seasonal reproduction in tropical as well as temperate-zone animals.