High-resolution geophysical imaging of reptile burrows (San Salvador rock iguana, The Bahamas): implications for ichnology and conservation ecology

Neoichnological research of terrestrial tracemakers in coastal settings provides important palaeoenvironmental information about their context within the subaerial facies. Here we present the first geophysical dataset of reptile burrows in a carbonate substrate and use it to help visualize parts of the burrows of the Bahamian (San Salvador) rock iguana (Cyclura rileyi). High-resolution 800 MHz ground-penetrating radar (GPR) images within an enclosure on San Salvador Island were employed to discriminate between the electromagnetic signal response from subsurface anomalies related to air-dominated voids or live animals within burrows. The dielectric contrast between the carbonate substrate and open burrows was sufficient to identify the majority of 15-20-cm-wide subsurface extensions of the inclined tunnels in the upper 30-40 cm. Whereas limestone clasts induced some interference, it is possible to differentiate their high-amplitude diffractions from those produced by the iguana burrows. Our research indicates that GPR imaging is a viable, rapid, non-invasive method of visualizing animal burrows, with implications to neoichnology, paleoichnology, and conservation ecology of semi-fossorial species. Furthermore, the critically endangered status of Bahamian land iguanas, as well as ongoing threats from natural and introduced pressures, highlights the need for research into their ichnological record.

Diversity begets diversity through shared adaptive genetic variation: discovery of a cryptic wide-mouthed scale-eater

Adaptive radiations involve astounding bursts of phenotypic, ecological, and species diversity. However, the microevolutionary processes that underlie the origins of these bursts are still poorly understood. We report the discovery of a cryptic intermediate wide-mouth scale-eating ecomorph in a recent radiation of Cyprinodon pupfishes which provides crucial information about the evolutionary and ecological transition from a widespread algae-eating generalist to a novel microendemic scale-eating specialist. We first show that this ecomorph occurs in sympatry with generalist C. variegatus and scale-eating specialist C. desquamator across several hypersaline lakes on San Salvador Island, Bahamas, but is genetically differentiated, morphologically distinct when reared in a common garden, and sometimes consumes scales. We then compared the timing of selective sweeps on shared and unique adaptive variants in both scale-eating species to characterize the evolutionary path to scale-eating. We predicted that adaptation to the intermediate wide-mouth scale-eating niche aided in the rapid divergence of the more specialized scale-eater C. desquamator. Therefore, selection for shared adaptive variants would occur first in wide-mouth. Contrary to our prediction, four of the six sets of shared adaptive alleles in both scale-eating species swept significantly earlier in C. desquamator. Adaptive introgression from the specialist into the wide-mouth ancestor may have resulted in parallel evolution of their dietary niche. Conversely, no adaptive alleles for scale-eating were reused in a third sympatric specialist C. brontotheriodes, despite sharing 9% of hard selective sweeps. Our work provides a microevolutionary framework for investigating how diversity begets diversity during adaptive radiation.

A vertebrate adaptive radiation is assembled from an ancient and disjunct spatiotemporal landscape

To investigate the origins and stages of vertebrate adaptive radiation, we reconstructed the spatial and temporal histories of adaptive alleles underlying major phenotypic axes of diversification from the genomes of 202 Caribbean pupfishes. On a single Bahamian island, ancient standing variation from disjunct geographic sources was reassembled into new combinations under strong directional selection for adaptation to the novel trophic niches of scale-eating and molluscivory. We found evidence for two longstanding hypotheses of adaptive radiation: hybrid swarm origins and temporal stages of adaptation. Using a combination of population genomics, transcriptomics, and genome-wide association mapping, we demonstrate that this microendemic adaptive radiation of novel trophic specialists on San Salvador Island, Bahamas experienced twice as much adaptive introgression as generalist populations on neighboring islands and that adaptive divergence occurred in stages. First, standing regulatory variation in genes associated with feeding behavior (prlh, cfap20, and rmi1) were swept to fixation by selection, then standing regulatory variation in genes associated with craniofacial and muscular development (itga5, ext1, cyp26b1, and galr2) and finally the only de novo nonsynonymous substitution in an osteogenic transcription factor and oncogene (twist1) swept to fixation most recently. Our results demonstrate how ancient alleles maintained in distinct environmental refugia can be assembled into new adaptive combinations and provide a framework for reconstructing the spatiotemporal landscape of adaptation and speciation.

Forty-year natural history study of Bahalana geracei Carpenter, 1981, an anchialine cave-dwelling isopod (Crustacea, Isopoda, Cirolanidae) from San Salvador Island, Bahamas: reproduction, growth, longevity, and population structure

Almost nothing has been reported on the natural history of any of the world’s 92 species of cave cirolanids, including those from saltwater caves (anchialine). Over 1400 specimens of Bahalana geracei Carpenter, 1981 were collected in two caves from 1978–2018; size-frequency data provided insight into population structure. Some specimens were maintained alive over multiple years to study rarely reported activities for cave cirolanids: feeding, molting, growth, longevity, and reproduction. Photographs document these phenomena. Mating occurred after gravid females shed both halves of reproductive molts. Females can have multiple broods (iteroparous) with ~2.0–3.5 years per reproductive cycle: egg production (~9–24 months), mating, brooding (5–6 months), release of 6–55 mancas (2.3–3.3 mm long), and oostegite molt (~2–13 months after manca release). Estimated lifetime fecundity is 58 mancas per female; probable range is 20–120. In Lighthouse Cave, females outnumbered males (~4:1), grew larger (16.8 vs. 9.5 mm), and lived longer. Growth rates were slow: ~1–2 years for three instars of post-marsupial manca development (from ~2.3–4.0 mm); estimated adult growth rate was 0.8 mm/year (1.6 molts/year) for males, and 0.5 mm/year (1.5 molts/year) for females. Longevity estimates for females are 25–28 years with 23–30 instars, vs. 6–8 years for males with 13–15 instars. Males from Major’s Cave were nearly as numerous and as large (14.8 mm) as females; estimated longevity for males is >20 years. Longevity estimates of >20 years appear to be the longest for any isopod species. Female longevity probably increased by being starvation resistant, surviving multiple broods, cannibalizing smaller B. geracei, and living in a low-stress environment. Populations appear to be stable, relatively large, and not currently threatened.

First known trace fossil of a nesting iguana (Pleistocene), The Bahamas

Most species of modern iguanas (Iguania, Iguanidae) dig burrows for dwelling and nesting, yet neither type of burrow has been interpreted as trace fossils in the geologic record. Here we describe and diagnose the first known fossil example of an iguana nesting burrow, preserved in the Grotto Beach Formation (Early Late Pleistocene, ~115 kya) on San Salvador Island, The Bahamas. The trace fossil, located directly below a protosol, is exposed in a vertical section of a cross-bedded oolitic eolianite. Abundant root traces, a probable land-crab burrow, and lack of ghost-crab burrows further indicate a vegetated inland dune as the paleoenvironmental setting. The trace fossil matches dimensions and overall forms of burrows made by modern iguanas, and internal structures indicate active backfilling consistent with modern iguana nesting burrows. The trace fossil is also located on an island with a modern native species of rock iguana (Cyclura riyeli riyeli), suggesting a presence of iguanas on San Salvador since the Late Pleistocene. This nesting burrow may provide a search image for more fossil iguana burrows in The Bahamas and other places with long-established iguana species and favorable geological conditions for preserving their burrows.