Ecological constraints associated with genome size across salamander lineages

Abstract

Salamanders have some of the largest, and most variable, genome sizes among the vertebrates. Larger genomes have been associated with larger cell sizes, lower metabolic rates, and longer embryonic and larval durations in many different taxonomic groups. These life-history traits are often important for dictating fitness under different environmental conditions, suggesting that a species' genome size may have the potential to constrain its ecological distribution. We test how genome size varies with the ephemerality of larval habitat across the salamanders, predicting that species with larger genomes will be constrained to more permanent habitats that permit slower development, while species with smaller genomes will be more broadly distributed across the gradient of habitat ephemerality. We found that salamanders with larger genomes are almost exclusively associated with permanent aquatic habitats. In addition, the evolutionary transition rate between permanent and ephemeral larval habitats is much higher in salamander lineages with smaller genome sizes. These patterns suggest that genome size may act as an evolutionary constraint on the ecological habitats of salamanders, restricting those species with large genomes and slower development to habitats with permanent sources of water.

Genome Size Covaries More Positively with Propagule Size than Adult Size: New Insights into an Old Problem

“…According to this view, small genomes are associated with r-selected traits, such as high colonizing ability, rapid individual and population growth, early maturation, high reproductive output and short lives that are favored in unstable or ephemeral habitats and at low population densities, whereas large genomes are associated with K-selected traits, such as high competitive ability, slower individual and population growth, late maturation, low reproductive output and long lives that are favored in stable habitats and at high population densities. Although the theory of r- and K-selection may help explain some variation in genome sizes (e.g., the association of large genomes with relatively slow growth rates and long lives in some protists, plants and ectothermic animals (e.g., [ 7 , 8 , 15 , 19 , 59 , 60 , 113 , 151 , 177 , 186 , 189 , 195 , 243 , 255 , 293 , 300 , 308 , 309 , 310 , 311 , 312 ]; but not in endothermic vertebrates [ 95 ]), and the association of relatively large genomes with larger, but fewer reproductive propagules ([ 146 , 166 , 217 , 219 , 313 , 314 ]; Table A2 ), it cannot explain why genome size covaries with body size in some taxa, but not others (as observed in Table 1 ).…”

“…Changes in genome size may not only result from life-history changes, but also cause them [ 103 ]. Variation in genome size is often (but not always) associated with changes in various life-history traits, including not only propagule size and number, but also growth rate, duration of developmental periods, and age at sexual maturity ([ 8 , 9 , 10 , 11 , 15 , 16 , 19 , 32 , 48 , 57 , 58 , 59 , 60 , 80 , 97 , 103 , 109 , 113 , 177 , 186 , 189 , 192 , 195 , 255 , 293 , 294 , 308 , 309 , 310 , 311 , 312 , 313 , 314 , 317 ]; see also sources cited in Table 2 ; but for contradictory evidence, see [ 97 , 98 ]). Interspecific correlations between genome size and longevity have also been proposed [ 48 ], but questioned [ 9 , 97 ].…”

Repeated ecological and life cycle transitions make salamanders an ideal model for evolution and development

“…31 The need for rapid development in ephemeral environments has been suggested as a reason why some biphasic amphibians maintain a relatively small genome size. 161,162 At the same time, lower developmental rate due to increased genome size may facilitate transitions to simple life cycles (direct developers and paedomorphs). 130,163,164 In salamanders, simpler life cycles permit genomic expansion which could have potential physiological advantages or could be a drift related process caused by relaxed selection, 165,166 or reduced mutational hazard.…”

Shedding light upon the complex net of genome size, genome composition and environment in chordates

“…The expansion of the lissamphibian genome would have started in the Permian before the separation of urodeles from anurans and the expansion of the urodeles genome, due to a few LTR families, would have continued in the early and Middle Triassic (Laurin et al 2015;Christoph-Liedtke 2016). The first phase of the expansion took place gradually and led to larger genomes in anuran; the next phase would have occurred because of the LTR retrotransposon saltatory proliferation (Sun & Mueller 2014) and would have led to very large genomes typical of current urodeles already in the Middle Jurassic (Laurin et al 2015;Organ et al 2015;Christoph-Liedtke et al 2018).…”

“…The relationship between genome size and the related developmental duration can represent a limiting factor in environment adaptation, especially concerning temperature and water availability. Indeed it has been observed that in amphibians, especially in anurans, species that live in environments characterized by scarcity of water have a small genome and a rapid development, while species that live in cold environments with water availability have larger genomes and a slow development (Goin et al 1968;McMenamin & Hadly 2010); similarly in urodeles species living in cold environments have a larger genome and a longer duration of development compared to species living in warmer environments (Litvinchuk et al 2006;Lertzman-Leofsky et al 2019). Similar correlations have also been reported for some fishes (Hardie & Hebert 2003, 2004.…”