Integrating patterns of thermal tolerance and phenotypic plasticity with population genetics to improve understanding of vulnerability to warming in a widespread copepod

Abstract

8Differences in population vulnerability to warming are defined by spatial patterns in thermal 9 adaptation. These patterns may be driven by natural selection over spatial environmental 10 gradients, but can also be shaped by gene flow, especially in marine taxa with high dispersal 11 potential. Understanding and predicting organismal responses to warming requires disentangling 12 the opposing effects of selection and gene flow. We begin by documenting genetic divergence of 13 thermal tolerance and developmental phenotypic plasticity. Ten populations of the widespread 14 copepod Acartia tonsa were collected from sites across a large thermal gradient, ranging from 15 the Florida Keys to Northern New Brunswick, Canada (spanning over 20 degrees latitude). 16Thermal performance curves from common garden experiments revealed local adaptation at the 17 sampling range extremes, with thermal tolerance increasing at low latitudes and decreasing at 18 high latitudes. The opposite pattern was observed in phenotypic plasticity, which was strongest 19 at high latitudes. Over a large portion of the sampled range, however, we observed a remarkable 20 lack of differentiation of thermal performance curves. To examine whether this lack of 21 divergence is the result of selection for a generalist performance curve or constraint by gene 22 flow, we analyzed cytochrome oxidase I mtDNA sequences, which revealed abundant genetic 23 2 diversity and widely-distributed haplotypes. Strong divergence in thermal performance within 24 genetic clades, however, suggests that the pace of thermal adaptation can be relatively rapid. The 25 combined insight from the laboratory physiological experiments and genetic data indicate that 26 gene flow constrains differentiation of thermal performance curves. This balance between gene 27 flow and selection has implications for patterns of vulnerability to warming. Taking both genetic 28 differentiation and phenotypic plasticity into account, our results suggest that local adaptation 29 does not increase vulnerability to warming, and that low latitude populations in general may be 30 more vulnerable to predicted temperature change over the next century. 31

Phylogeography of Acartia tonsa Dana, 1849 (Calanoida: Copepoda) and phylogenetic reconstruction of the genus Acartia Dana, 1846

“…They show the presence of four major clades. This is in agreement with our observations where the four corresponding clades would presumably be clades III (S), V, VI (X), and VII (F), note that clade IV in our study is only found in Texas and Brazil, not sampled by Sasaki and Dam (2019). In their study, they analyze their data under the assumption that these clades are the same species and treat their samples from each location as a population.…”

“…Making such distinctions are essential before undertaking any population-specific study on A. tonsa. For example, a recent study by Sasaki and Dam (2019) investigated patterns of thermal tolerance and phenotypic plasticity in A. tonsa. They collected specimens of A. tonsa from the Northwest Atlantic (north of 40°N) and Florida (south of 30°N) including coasts in the Atlantic and the Gulf of Mexico.…”

“…They show how the various mtCOI clades of Acartia are widespread with some sites sharing haplotypes and how thermal tolerance decreases at higher latitudes, while phenotypic plasticity increases. One of their main conclusions is that the large plasticity in A. tonsa results in the wide geographic distribution of this species in varying environmental conditions and that this, combined with high levels of genetic diversity increases migration success and reduces vulnerability to stressors such as climate change (Sasaki and Dam 2019). Evidence from the present study and previous research indicates that these lineages are not the same species (e.g., Caudill and Bucklin 2004;Hare 2008, 2011;Plough et al 2018) and each has its own evolutionary history and likely has been influenced by different speciation processes.…”

“…In the case of Sasaki and Dam (2019) if each of the four major lineages is analyzed independently as four distinct species, geographic structuring becomes readily apparent and estimated gene flow between the various locations would be reduced. For example, Sasaki and Dam (2019) show that the specimens from lower latitudes largely belong to lineages A and B which are infrequent in northern sites (absent in the case of lineage A in the 3 northernmost sites), with one and zero haplotypes shared between northern and southern sites respectively. Specimens from lineage D and C are mostly found in northern sites, they are only present in low numbers in one and two of the five southern sites respectively.…”

“…Acartia tonsa Dana, 1849, is a calanoid copepod (Copepoda:Calanoida) in the family Acartiidae that is commonly found in coastal estuaries. Acartia tonsa is one of the most abundant and well-studied copepods in the world (Caudill and Bucklin 2004;Hare 2008, 2011;da Costa et al 2011;da Costa et al 2014;Zhou et al 2016;Werbrouck et al 2016;Minh et al 2017;Øie et al 2017;Rahlff et al 2017;Franco et al 2017;Jepsen et al 2017;Pavlaki et al 2017;Krause et al 2017;Plough et al 2018;Gomes et al 2018;Sasaki and Dam 2019) with a global distribution along the coasts of the Indo-Pacific and Atlantic (Mauchline et al 1998). It is often the dominant copepod species in estuaries playing a vital role in the trophic dynamics of these ecosystems as the main consumer of phytoplankton and the main food source for varied fish species (Mauchline et al 1998).…”