Showing papers by "Jonathan B. Losos published in 2021"

The Evolution of 'Ecological Release' into the 21st Century.

Abstract: Ecological release, originally conceived as niche expansion following a reduction in interspecific competition, may prompt invasion success, morphological evolution, speciation, and other ecological and evolutionary outcomes. However, the concept has not been recently reviewed. Here, we trace the study of 'ecological release' from its inception through the present day and find that current definitions are broad and highly varied. Viewing this development as a potential impediment to clear communication and hypothesis testing, we suggest a consensus definition for ecological release: niche expansions and shifts when a constraining interspecific interaction is reduced or removed. In rationalizing this definition, we highlight the various ways ecological release can unfold and address its potential evolutionary consequences.

Habitat structure mediates vulnerability to climate change through its effects on thermoregulatory behavior

Abstract: Tropical ectotherms are thought to be especially vulnerable to climate change because they are thermal specialists, having evolved in aseasonal thermal environments. However, even within the tropics, habitat structure can influence opportunities for behavioral thermoregulation. Open (and edge) habitats likely promote more effective thermoregulation due to the high spatial heterogeneity of the thermal landscape, while forests are thermally homogenous and may constrain opportunities for behavioral buffering of environmental temperatures. Nevertheless, the ways in which behavior and physiology interact at local scales to influence the response to climate change are rarely investigated. We examined the thermal ecology and physiology of two lizard species that occupy distinct environments in the tropics. The brown anole lizard (Anolis sagrei) lives along forest edges in The Bahamas, whereas the Panamanian slender anole (Anolis apletophallus) lives under the canopy of mature forests in Panama. We combined detailed estimates of environmental variation, thermoregulatory behavior, and physiology to model the vulnerability of each of these species. Our projections suggest that forest-dwelling slender anoles will experience severely reduced locomotor performance, activity time, and energy budgets as the climate warms over the coming century. Conversely, the forest-edge-dwelling brown anoles may use behavioral compensation in the face of warming, maintaining population viability for many decades. Our results indicate that local habitat variation, through its effects on behavior and physiology, is a major determinant of vulnerability to climate change. When attempting to predict the impacts of climate change on a given population, broad-scale characteristics such as latitude may have limited predictive power.

Chromosome-scale genome assembly of the brown anole (Anolis sagrei), a model species for evolution and ecology

Abstract: Rapid technological improvements are democratizing access to high quality, chromosome-scale genome assemblies. No longer the domain of only the most highly studied model organisms, now non-traditional and emerging model species can be genome-enabled using a combination of sequencing technologies and assembly software. Consequently, old ideas built on sparse sampling across the tree of life have recently been amended in the face of genomic data drawn from a growing number of high-quality reference genomes. Arguably the most valuable are those long-studied species for which much is already known about their biology; what many term emerging model species. Here, we report a new, highly complete chromosome-scale genome assembly for the brown anole, Anolis sagrei – a lizard species widely studied across a variety of disciplines and for which a high-quality reference genome was long overdue.

When adaptive radiations collide: Different evolutionary trajectories between and within island and mainland lizard clades

Abstract: Oceanic islands are known as test tubes of evolution. Isolated and colonized by relatively few species, islands are home to many of nature's most renowned radiations from the finches of the Galapagos to the silverswords of the Hawaiian Islands. Despite the evolutionary exuberance of insular life, island occupation has long been thought to be irreversible. In particular, the presumed much tougher competitive and predatory milieu in continental settings prevents colonization, much less evolutionary diversification, from islands back to mainlands. To test these predictions, we examined the ecological and morphological diversity of neotropical Anolis lizards, which originated in South America, colonized and radiated on various islands in the Caribbean, and then returned and diversified on the mainland. We focus in particular on what happens when mainland and island evolutionary radiations collide. We show that extensive continental radiations can result from island ancestors and that the incumbent and invading mainland clades achieve their ecological and morphological disparity in very different ways. Moreover, we show that when a mainland radiation derived from island ancestors comes into contact with an incumbent mainland radiation the ensuing interactions favor the island-derived clade.

Changes in selection pressure can facilitate hybridization during biological invasion in a Cuban lizard

Abstract: Hybridization is among the evolutionary mechanisms most frequently hypothesized to drive the success of invasive species, in part because hybrids are common in invasive populations. One explanation for this pattern is that biological invasions coincide with a change in selection pressures that limit hybridization in the native range. To investigate this possibility, we studied the introduction of the brown anole (Anolis sagrei) in the southeastern United States. We find that native populations are highly genetically structured. In contrast, all invasive populations show evidence of hybridization among native-range lineages. Temporal sampling in the invasive range spanning 15 y showed that invasive genetic structure has stabilized, indicating that large-scale contemporary gene flow is limited among invasive populations and that hybrid ancestry is maintained. Additionally, our results are consistent with hybrid persistence in invasive populations resulting from changes in natural selection that occurred during invasion. Specifically, we identify a large-effect X chromosome locus associated with variation in limb length, a well-known adaptive trait in anoles, and show that this locus is often under selection in the native range, but rarely so in the invasive range. Moreover, we find that the effect size of alleles at this locus on limb length is much reduced in hybrids among divergent lineages, consistent with epistatic interactions. Thus, in the native range, epistasis manifested in hybrids can strengthen extrinsic postmating isolation. Together, our findings show how a change in natural selection can contribute to an increase in hybridization in invasive populations.

The anoles of la selva: niche partitioning and ecological morphology in a mainland community of anolis lizards

Abstract: Describing the relationships among morphology, behavior, and ecology is central to understanding the processes of evolutionary diversification. Anolis lizards are an excellent group for studying such ecomorphological relationships. Extensive research on anole ecological morphology has been conducted in the Caribbean, where sympatric species have repeatedly and convergently evolved to partition habitat through differential perch use. Six ecomorphs have been described, each with particular behavioral, morphological, and ecological characteristics well-suited for the microhabitat it occupies. However, little research has been conducted in mainland Central or South America, and a few case studies suggest that mainland anoles may not conform to the ecomorph classes recognized for Greater Antillean anoles. In this study, we examine the ecological morphology of sympatric mainland species of Anolis in a tropical lowland rainforest in Costa Rica and compare these species to the Caribbean ecomorphs. Our results show overlapping niches and substantial variability in habitat use across many species. Moreover, the relationship between relative hindlimb morphology and habitat use in Anolis humilis and Anolis limifrons does not conform to that of Caribbean species. Predation and fluctuating environmental conditions likely structure morphological variation differently in the mainland, leading the independent radiation of mainland anoles to produce divergent ecomorphological relationships compared with the Caribbean islands.

What Determines Paternity in Wild Lizards? A Spatiotemporal Analysis of Behavior and Morphology

Abstract: Mating behavior in animals can be understood as a sequence of events that begins with individuals encountering one another and ends with the production of offspring. Behavioral descriptions of animal interactions characterize early elements of this sequence, and genetic descriptions use offspring parentage to characterize the final outcome, with behavioral and physiological assessments of mates and mechanisms of copulation and fertilization comprising intermediate steps. However, behavioral and genetic descriptions of mating systems are often inconsistent with one another, complicating expectations for crucial aspects of mating biology, such as the presence of multiple mating. Here, we use behavioral and genetic data from a wild population of the lizard Anolis cristatellus to characterize female multiple mating and the potential for sexual selection through female mate choice in this species. We find that 48% of sampled females bore offspring sired by multiple males. Moreover, spatiotemporal proximity between males and females was associated with whether a male sired a female's offspring, and if yes, how many offspring he sired. Additionally, male body size, but not display behavior, was associated with reproductive outcomes for male-female pairs. While much remains to be learned about the mechanisms of mating and targets of sexual selection in A. cristatellus, it is clear that female multiple mating is a substantial component of this species' mating system in nature.

Conservation and convergence of genetic architecture in the adaptive radiation of Anolis lizards

Abstract: The G matrix, which quantifies the genetic architecture of traits, is often viewed as an evolutionary constraint. However, G can evolve in response to selection and may also be viewed as a product of adaptive evolution. The evolution of similar G matrices in similar environments would suggest that G evolves adaptively, but it is difficult to disentangle such effects from phylogeny. Here, we use the adaptive radiation of Anolis lizards to ask whether convergence of G accompanies the repeated evolution of habitat specialists, or ecomorphs, across the Greater Antilles. We measured G in seven species representing three ecomorphs (trunk-crown, trunk-ground, and grass-bush). We found that the overall structure of G does not converge. Instead, the structure of G is well conserved and displays a phylogenetic signal. However, several elements of G showed signatures of convergence, indicating that some aspects of genetic architecture have been shaped by selection. Most notably, genetic correlations between limb traits and body traits were weaker in long-legged trunk-ground species, suggesting effects of recurrent selection on limb length. Our results demonstrate that common selection pressures may have subtle but consistent effects on the evolution of G, even as the overall pattern of genetic architecture remains conserved.