Evolution of reproductive behavior in Ambystomatid salamanders
The variable egg-laying strategies and parental care of the salamander genus, Ambystoma, provides an excellent system in which to examine the process through which reproductive behavior evolves. Research projects in my lab have compared embryonic development between aquatic and terrestrial egg-layers and have quantified gene expression in the brains of mating-phase and parenting-phase females. Most recently, we are developing genetics tools to describe mating systems across multiple species.
Variation in embryonic development
Phylogenies of the Ambystoma strongly support aquatic egg-laying and absence of parental care as ancestral in this group. Terrestrial egg-laying has evolved independently twice and parental care just once, in the marbled salamander, A. opacum. Parental care in A. opacum may have evolved as a by-product of selection for more competitive larvae. Strong selection to be the earliest larvae to hatch may have driven the evolution of terrestrial eggs that are ready to hatch as soon as water arrives. As in terrestrial egg-layers of other salamander taxa, terrestrial eggs are associated with parental care in A. opacum. In contrast, most Ambystoma lay their eggs in water and do not provide care.
We examined developmental and life history traits of embryos to determine whether a shift toward earlier, fall breeding, as in A. opacum and the ringed salamander, A. annulatum, coincides with prolonged development relative to winter-breeding species. Our hypothesis is that winter and spring breeding species have less time to develop to metamorphosis than fall breeders, and this may select for faster development not only in the larval stage but also in the embryos. We compared embryonic development of A. opacum and A. annulatum to that of the winter-breeding spotted salamander, A. maculatum, and found that A. opacum, but not A. annulatum, showed evidence of prolonged embryonic development. These results were not consistent with our hypothesis of early breeding relaxing selection for fast development. Rather, the results suggest that terrestrial egg-laying or parental care – both traits of A. opacum – could alter selection on embryonic growth.
This work was performed in collaboration with Caroline Kennedy and undergraduates Natrieifia Miller (UNCA ’17), Tony Francis (UNCA ’15), and Kimberly Treadaway (UNCA ’20).
Maintenance of an egg mass polymorphism in Ambystoma maculatum
Genetic polymorphisms that produce different yet co-occurring phenotypes can be difficult to explain – if one phenotype confers even slightly higher fitness, the less favorable phenotype and allele(s) will become locally extinct. When polymorphisms are widespread, with morphs co-occurring across a range of abiotic and biotic conditions, there must exist processes that favor both morphs in the same population. The spotted salamander, Ambystoma maculatum, exhibits an egg mass polymorphism in which females produce masses with either white or clear jelly. The polymorphism is understood to be the result of a single locus polymorphism.
With Caroline Kennedy and undergraduates Danielle Winkelman (UNCA ’15), Elsea Brown (UNCA ’16), Laura Fullmer (UNCA ’19), and Mischa D’Errico (UNCA ’18), we have been examining the hypothesis that the egg mass polymorphism is maintained via spatial and temporal heterogeneity in both predation risk and abiotic variables.
White egg mass morphs appear to have a survival advantage in the presence of newts and wood frogs, as these masses are less likely to be nibbled on by these predators. This apparent advantage of white masses may be balanced by an advantage to clear masses if they are better hosts for the symbiotic alga, Oophila amblystomatis. Although cold water temperatures during A. maculatum’s breeding season slow embryonic development , interior embryos often develop more slowly than exterior embryos, as the rate of oxygen diffusion to interior embryos is limited by the egg mass jelly . The problem of oxygen diffusion is solved by the alga, which is both endo- and ecto-symbiotic.
In seasons and populations with high predator densities, the white morph may have higher fitness owing to higher predation on clear masses, whereas the clear morph may have higher fitness where embryonic oxygen demands are more acute. In water that is either warmer or lower in dissolved oxygen, algae may increase oxygen availability sufficiently to maintain constant developmental rates. However, growth of algae may depend on opacity of egg mass jelly and clear masses may transmit more light to algae than white masses.
Phytotelma communities of pitcher plants in rare Western North Carolina mountain bogs
In the mountains of Western North Carolina are situated numerous bogs and fens that harbor a wide variety of rare bog plants and animals, including multiple endemic varieties of pitcher plants in the genus, Sarracenia. Bogs and fens have low nutrient availability and pitcher plants have evolved carnivory as a means of gaining nutrients lacking in soil. Pitcher plants have tubular leaves that secrete or capture water and produce attractants that lure insects. When insects enter, they become trapped and drown. Although many species produce enzymes that digest drowned insects, a few rely on other organisms to break down their prey. Sarracenia purpurea and its mountain endemic, S. purpurea var. montana, go a step further by harboring a diverse community of symbiotic organisms, including bacteria, rotifers, nematodes, and mosquitoes. This is referred to as phytotelma community (one within a contained pool of water). Pitcher plant species that harbor phytotelma communities instead absorb nutrients released as the symbionts feed and grow.
Effects of hybridization and isolation on phytotelma communities
Hybridization may be particularly detrimental in pitcher plants (Sarracenia sp.) and to the invertebrates that live within them. Members of the genus Sarracenia are found in 50 of North Carolina’s 100 counties, and this group is notable for the ease with which congeneric hybridization occurs. In two local mountain seeps, Sarracenia purpurea L. ssp. purpurea var. montana Schnell & Determann seems to co-occur with Sarracenia rubra Walter ssp. jonesii (Wherry), a taxon found only in North and South Carolina. The threat for pitcher plants caused by hybridization stems from their diverse means of obtaining nutrients. Hybrids between a carnivorous (S. rubra ssp. jonesii) and a non-carnivorous (S. purpurea var. montana) species could have pitcher environments that are both inhospitable to colonizing symbionts and inefficient at digesting trapped prey. This could lead to selection on symbionts to avoid hybrids, further limiting the ability of hybrids to obtain necessary nutrients.
With colleagues Jennifer Rhode Ward and Caroline Kennedy, and undergraduates Steve Jaslow (UNCA ’14), Elise Powell (UNCA ’16), Lila Uzell (UNCA ’17), Leila Beikmohamadi (UNCA ’18), Miranda Satterfield (UNCA ’16), Wayne Morgan (UNCA ’20), and Ally Brandon (UNCA ’19), we have been comparing phytotelma communities and reproductive traits between S. purpurea var. montana, S. rubra ssp. jonesii, and hybrids.
Not only are populations of these two species typically small in the mountains, but the bog ecosystems in which they live are rare. As a result, mountain bogs may function like ecosystem islands in which species diversity and population dynamics are largely dependent on the ability of organisms to colonize and persist. Again with colleagues Jennifer Rhode Ward and Caroline Kennedy, and undergraduates Elise Powell (UNCA ’16), Lila Uzell (UNCA ’17), Leila Beikmohamadi (UNCA ’18), and Wayne Morgan (UNCA ’20), we are examining interpopulation variation in phytotelma community structure and we are examining whether community size or structure varies with the degree of population isolation or with plant population size.